Microbiota refers to the assemblage of microorganisms, including bacteria, archaea, eukaryotes, and viruses, present in a defined environment such as the human body, animal guts, plant rhizospheres, or soil niches.[1] In humans, the microbiota comprises an estimated 10 to 100 trillion microbial cells that coexist symbiotically with host cells, primarily inhabiting the gastrointestinal tract but also sites like the skin, oral cavity, and respiratory system.[2] These microbial communities have co-evolved with humans over millennia, influencing physiology, metabolism, and immune function while being shaped by factors such as diet, environment, and antibiotics.[3]A key distinction exists between microbiota and microbiome: the former denotes the collective microorganisms themselves, while the latter encompasses the microbiota along with their genomes (the metagenome) and the surrounding environmental conditions within the host.[1] This broader microbiome perspective highlights the vast genetic diversity it imparts; for instance, the human gut microbiome alone encodes approximately 10 million non-redundant genes, dwarfing the roughly 20,000 genes in the human genome.[4] The term "microbiota" supplanted outdated concepts like "microflora," which implied a plant-like composition, and its study relies on molecular techniques such as 16S rRNA gene sequencing to characterize microbial diversity.[1]The composition of the human microbiota is dominated by bacteria, particularly from phyla such as Firmicutes and Bacteroidetes in the gut, which together account for over 90% of the bacterial population, alongside smaller contributions from Actinobacteria, Proteobacteria, and others.[5]Archaea, fungi, protozoa, and viruses form minor but functionally significant components, with the gut harboring around 10¹¹ to 10¹² microbial cells per gram of content and an overall bacterial cell count estimated at 3.8 × 10¹³ per individual, roughly matching the number of human cells.[3] Diversity varies by body site: the gut microbiota is the most abundant and diverse, while skin and oral microbiotas are adapted to drier or more exposed conditions, featuring genera like Streptococcus and Staphylococcus.[5] Across individuals, microbiota profiles are highly personalized, influenced by genetics, age, and lifestyle, yet exhibit functional redundancy where similar metabolic roles are performed by different species.[2]Functionally, the microbiota performs essential roles in host nutrition and protection. It ferments undigested dietary fibers into short-chain fatty acids (SCFAs) like butyrate, which provide energy to colonocytes and regulate inflammation; synthesizes vitamins such as B and K; and metabolizes bile acids, drugs, and xenobiotics.[5] In immune modulation, microbiota-derived signals via Toll-like receptors (TLRs) and secretory immunoglobulin A (sIgA) promote barrier integrity, train immune cells, and prevent pathogen colonization, thereby maintaining homeostasis.[3] These interactions extend to the brain-gut axis, where microbial metabolites influence neurological function, underscoring the microbiota's systemic impact.[5]Dysbiosis—an imbalance in microbiota composition—has been linked to numerous diseases, including inflammatory bowel disease, obesity, diabetes, and even neurological disorders like depression, through mechanisms such as altered metabolite production and chronic inflammation.[5] Conversely, a healthy microbiota supports disease resistance and therapeutic responses, with interventions like fecal microbiota transplantation (FMT), probiotics, and prebiotics showing promise in restoring balance.[5] Ongoing research emphasizes the microbiota's role in personalized medicine, as its plasticity offers avenues for modulating health outcomes across diverse populations.[2]
Definition and Fundamentals
Definition and Scope
Microbiota refers to the assemblage of microorganisms, including bacteria, archaea, and eukaryotic microorganisms such as fungi and protozoa, present in a particular environment, with a particular emphasis on communities associated with multicellular hosts.[6] This term encompasses the collective living microbial populations that inhabit specific niches, such as those within or on host organisms, where they form complex, dynamic communities. The word "microbiota" derives from Ancient Greek roots: "micros" meaning small, and "biota" as the plural of "bios," meaning life.[6]A key distinction exists between microbiota and the related term microbiome. While microbiota denotes the actual microorganisms themselves—their cells, structures, and interactions—the microbiome extends to include the collective genomes of these microbes (the metagenome) along with surrounding environmental components, such as metabolites and habitat features that influence microbial activity.[6] This broader conceptualization of the microbiome highlights not only the composition of the microbial community but also its functional and genetic potential within the ecosystem.The scope of microbiota spans diverse environments, broadly categorized into host-associated and free-living forms. Host-associated microbiota, such as those in the gut or on the skin of animals, or in plant roots, are intimately linked to their hosts and often exhibit specialized adaptations for colonization and persistence.[7] In contrast, free-living microbiota inhabit non-host settings like soil, water, or air, where they interact within broader ecological networks without direct host dependency.[7] Central to understanding microbiota are concepts like diversity metrics: alpha diversity measures the richness and evenness of microbial species within a single sample, while beta diversity quantifies differences in composition between samples or communities.[8] Furthermore, microbiota composition is profoundly shaped by host phylogeny, which determines evolutionary relatedness, and ecological factors, such as diet, habitat, and environmental pressures, leading to predictable patterns across taxa.[9]
Historical Context and Discovery
The earliest observations of microorganisms, which laid the groundwork for understanding microbiota, were made by Antonie van Leeuwenhoek in the late 17th century using his self-designed single-lens microscopes. In 1683, Leeuwenhoek reported the first sighting of bacteria, describing "animalcules" in samples of dental plaque scraped from his own teeth and those of others, revealing a previously invisible world of microbial life in the human mouth.[10] These discoveries, detailed in letters to the Royal Society and published in 1684, marked the initial recognition of microbes as ubiquitous entities, though their ecological roles remained unexplored for centuries.[11]In the early 20th century, research shifted toward the biological significance of microbes in host health, pioneered by Ilya Mechnikov (also known as Élie Metchnikoff). Mechnikov's work on phagocytosis, for which he shared the 1908 Nobel Prize in Physiology or Medicine with Paul Ehrlich, demonstrated how immune cells engulf and destroy pathogens, establishing the cellular basis of innate immunity and highlighting microbes' dual role as threats and regulators.[12] Building on this, in his 1907 book The Prolongation of Life: Optimistic Studies, Mechnikoff proposed that certain gut bacteria, such as those in fermented milk like yogurt, could promote longevity by counteracting harmful intestinal putrefaction, introducing early concepts of probiotics and beneficial microbiota.[13] These ideas, inspired by observations of long-lived populations consuming fermented foods, emphasized commensal microbes' potential to influence host aging and health.[14]By the mid-20th century, perspectives evolved from viewing microbes primarily as pathogens to recognizing their commensal and symbiotic contributions, culminating in Joshua Lederberg's introduction of the term "microbiome" in 2001. In a commentary co-authored with Alexa T. McCray, Lederberg defined the microbiome as the ecological community of commensal, symbiotic, and pathogenic microorganisms inhabiting a host, underscoring the need to study these assemblages holistically rather than in isolation.[15] This coinage reflected a paradigm shift influenced by advances in genetics and ecology, framing microbiota as integral to host physiology. The term "microbiota" itself emerged in scientific literature in the early 1900s to describe microbial communities in specific environments.[5]The late 20th and early 21st centuries saw expanded microbial classification and diversity assessment through molecular techniques. In 1977, Carl Woese and George Fox's analysis of ribosomal RNA sequences revealed a third domain of life, Archaea, distinct from Bacteria and Eukarya, fundamentally reshaping the tree of life and acknowledging greater microbial phylogenetic complexity.[16] Subsequently, in the 1980s, Norman Pace developed culture-independent methods, such as environmental 16S rRNA gene sequencing, which demonstrated that over 99% of microbial diversity had been unculturable by traditional lab methods, unveiling vast, previously hidden ecosystems in natural and host-associated environments.[17] These innovations propelled microbiota research into a genomic era, emphasizing its ecological breadth.
Microbial-Host Interactions
Types of Relationships
The relationships between microbiota and their hosts span a spectrum of symbiotic interactions, as originally conceptualized by biologist Lynn Margulis in her framework of symbiosis as a fundamental driver of evolutionary biology.[18] In this spectrum, symbiosis refers to close, prolonged associations between organisms of different species, ranging from mutually beneficial to antagonistic. Margulis emphasized that such interactions often lead to integrated evolutionary outcomes, such as endosymbiosis, where one organism resides within another.[19]Symbiotic relationships can be classified as obligate or facultative based on the degree of dependency. Obligate symbiosis requires the association for the survival or reproduction of one or both partners, as seen in certain intracellular bacteria that cannot persist independently outside their host cells.[20] Facultative symbiosis, in contrast, allows partners to survive separately but provides advantages when together, enabling flexibility in microbial-host dynamics within diverse environments.[21]Mutualism represents a beneficial symbiosis where both the microbiota and host gain advantages, often involving reciprocal exchange of resources or services. For instance, gut bacteria in mammals ferment dietary fibers into short-chain fatty acids, providing energy to the host while receiving a protected niche and nutrients in return.[22] This interaction enhances host nutrition and immune function, underscoring mutualism's role in metabolic homeostasis.[23]Commensalism occurs when the microbiota benefits without significantly affecting the host, either positively or negatively. Transient microbes on the skin, such as certain Staphylococcus species, exemplify this by utilizing host-derived lipids for growth while imposing no detectable harm or benefit under normal conditions.[24] These associations maintain microbial diversity on epithelial surfaces, contributing to ecological balance without altering host physiology.[25]Parasitism and pathogenesis mark the antagonistic end of the spectrum, where microbiota derive benefits at the host's expense, potentially leading to disease. Opportunistic pathogens, like Candida albicans in the gut, typically reside as harmless commensals but can cause infections during host immunosuppression, invading tissues and eliciting inflammatory responses.[5] Such shifts highlight how environmental cues can transform neutral interactions into harmful ones, disrupting host health.[26]Central to understanding these relationships is the holobiont model, which views the host and its microbiota as a single ecological and evolutionary unit, rather than isolated entities.[27] Coined by Margulis and expanded in modern microbiology, this concept posits that the holobiont's fitness emerges from integrated interactions, influencing traits like resilience to stressors.[28]Microbial coordination within these relationships is facilitated by quorum sensing, a cell-to-cell communication mechanism where bacteria release and detect signaling molecules to synchronize behaviors based on population density.[29] In the gut microbiota, quorum sensing regulates processes like biofilm formation and virulence factor expression, enabling collective responses that shape host interactions.[30] This density-dependent signaling ensures adaptive group-level strategies, such as modulating pathogenesis or mutualistic contributions.[31]
Acquisition, Development, and Dynamics
Microbiota acquisition occurs through two primary mechanisms: vertical transmission, where microbes are passed directly from parent to offspring, and horizontal transmission, involving acquisition from the environment or other individuals. Vertical transmission typically begins during birth and early postnatal interactions, seeding the initial microbial community in the host. Horizontal transmission complements this by allowing ongoing colonization from external sources, such as food, water, and social contacts, which diversifies the microbiota over time.[32][33]In vertical transmission, maternal microbes are transferred to the offspring, often during vaginal delivery, where the neonate is exposed to the vaginal and fecal microbiota of the mother, establishing a foundational community dominated by species like Bifidobacterium and Lactobacillus. This process is crucial for initial colonization, particularly in the gut, and influences long-term microbial composition. For instance, in humans, cesarean section births reduce exposure to these maternal microbes, leading to altered initial seeding compared to vaginal births. Recent studies have demonstrated paternal contributions through seminal fluid and gut microbiota, influencing offspring microbiota seeding and health, in addition to close contact, further shaping the early microbiota.[34][35][36]Horizontal transmission enables the microbiota to adapt to the host's environment post-initial seeding, with microbes acquired through diet, hygiene practices, and interactions with conspecifics or surroundings. This mode is prominent in social animals, where sharing of food or grooming facilitates microbial exchange, promoting community resilience. In contrast to vertical transmission's specificity, horizontal pathways introduce a broader range of taxa, allowing for ecological succession as the host matures. Environmental factors, such as soil exposure in terrestrial hosts or water sources in aquatic ones, play key roles in this ongoing acquisition.[32][37]Developmental stages of the microbiota begin with pioneer species in neonates, which are often facultative anaerobes capable of thriving in low-oxygen, nutrient-scarce environments shortly after birth. These early colonizers, such as Enterobacteriaceae in the gut, pave the way for more complex communities by modifying the habitat through metabolite production and oxygen depletion. In humans, the microbiota undergoes rapid diversification in the first months, stabilizing into an adult-like composition by around age three, influenced by weaning and dietary shifts. This maturation follows a predictable trajectory across hosts, reflecting host physiology and environmental cues, though disruptions can delay succession.[38][39]Microbiota dynamics involve fluctuations driven by stability factors like host pH, nutrient availability, and immune responses, which maintain community equilibrium. Diet is a primary modulator, with fiber-rich intake promoting fermentative bacteria like Bacteroides, while high-fat diets favor bile-tolerant species, altering overall composition. Perturbations, such as sudden dietary changes, can induce dysbiosis—a shift toward imbalance—characterized by reduced diversity and overgrowth of opportunistic taxa. These dynamics highlight the microbiota's plasticity, enabling adaptation but also vulnerability to stressors.[40][41]Ecological succession models, drawn from broader community assembly theory, describe microbiota development as a deterministic process where pioneer species facilitate later arrivals through niche modification, akin to primary succession in ecosystems. Priority effects and dispersal limitation influence which taxa dominate, while stochastic elements like host genetics add variability. Resilience—the capacity to recover from perturbations—is governed by functional redundancy among taxa and network connectivity, allowing the community to rebound post-disruption, such as after dietary shifts. Studies applying these models underscore how early assembly shapes long-term stability, with resilient microbiomes exhibiting rapid compositional recovery.[42][43][44]
Host-Specific Microbiota
Human Microbiota
The human microbiota encompasses the trillions of microorganisms residing in and on the body, with estimates from the Human Microbiome Project (HMP) indicating approximately 3.8 × 10^{13} bacterial cells per individual, which predominantly comprise the microbiota (as estimated in 2016).[45][46] This microbial community varies significantly across body sites, influenced by factors such as age, sex, and geography, which shape its phyla-level diversity and functional roles.[47] For instance, aging is associated with shifts in microbial richness, particularly on the skin, while sex differences affect vaginal and gut compositions, and geographic location drives variations in overall gut microbiota structure due to dietary and environmental factors.[48][49][50]Major body sites host distinct microbial communities. The gut, the most densely populated site, contains around 3.8 × 10^{13} bacterial cells, which predominantly comprise the microbiota (as estimated in 2016), dominated by the phyla Firmicutes and Bacteroidetes, which together comprise over 90% of the bacterial population.[45][51] The skin microbiota is primarily composed of Actinobacteria (about 52% of bacteria), including genera like Propionibacterium and Corynebacterium, adapted to its dry, variable environment.[52] In the oral cavity, Streptococcus species predominate, contributing to high alpha diversity across sub-sites like the tongue and saliva.[53] The vaginal microbiota, in healthy individuals, is typically dominated by Lactobacillus species, which maintain low diversity and an acidic environment.[54]These microbial communities perform essential functions, including aiding digestion through the production of short-chain fatty acids (SCFAs) like butyrate and acetate by gut bacteria such as Bacteroides thetaiotaomicron, which ferment dietary fibers to provide energy to host cells.[47] Additionally, the microbiota modulates the immune system, with SCFAs influencing T-cell differentiation and responses; for example, Bacteroides fragilis-derived polysaccharides promote regulatory T-cell development, helping maintain immune homeostasis.[55] HMP analyses across 242 healthy adults revealed site-specific stability in these compositions, with 81–99% of predicted genera consistently identified, underscoring the personalized yet resilient nature of the human microbiota.[47]
Animal Microbiota
Animal microbiota exhibit significant diversity across taxa, shaped by physiological needs, ecological niches, and environmental factors, playing crucial roles in digestion, immunity, and osmoregulation. In mammals, gut communities are particularly adapted to dietary requirements, with herbivores hosting complex microbial consortia that facilitate the breakdown of fibrous plant material. For instance, ruminants like cows rely on foregut fermentation in the rumen, where methanogenic archaea such as Methanobrevibacter species convert hydrogen and carbon dioxide produced by bacterial fermentation into methane, contributing substantially to enteric emissions.[56] These archaea dominate the rumenmicrobiome, enabling efficient energy extraction from cellulose but also posing environmental challenges due to greenhouse gas production.[56]In contrast, hindgut fermenters such as horses depend on microbial activity in the cecum and colon for post-gastric digestion of forage, where bacteria and protozoa hydrolyze structural carbohydrates into volatile fatty acids, supplying over half of the horse's maintenance energy needs.[57] This fermentation process is sensitive to diet composition, with high-starch feeds potentially disrupting microbial balance and leading to acidosis.[57] Such adaptations highlight how mammalian gut microbiota evolve to support herbivory, differing markedly from the simpler communities in carnivores that prioritize protein and lipid metabolism.[58]Beyond mammals, non-mammalian animals display microbiota tailored to unique anatomical sites and functions. In fish, gill-associated microbes contribute to osmoregulation by aiding ion transport and maintaining epithelial integrity in varying salinities, with bacterial communities responding to osmotic gradients to support host acclimation.[59] Endogenous symbionts in fish gills facilitate ammonia oxidation and nutrient cycling, enhancing survival in hydrochemically diverse habitats.[60] Similarly, in arthropods, the endosymbiontWolbachia profoundly influences reproduction through mechanisms like cytoplasmic incompatibility and male killing, ensuring vertical transmission and altering host population dynamics across insect and crustacean species.[61]Microbiota composition in animals varies markedly with diet and habitat, underscoring their plasticity. Herbivores generally harbor higher microbial diversity than carnivores, with gut communities in the former enriched for fiber-degrading taxa like Firmicutes and Bacteroidetes, while carnivores feature proteolysis-specialized microbes such as Fusobacteria.[58] This dietary divergence drives functional specialization, where herbivore microbiomes emphasize polysaccharide utilization and carnivore ones focus on amino acid breakdown.[58]Habitat also exerts strong influence; aquatic animals, including fish, exhibit microbiomes more aligned with surrounding water chemistry than phylogenetic relatedness, with salinity and oxygen levels shaping gill and gut assemblages differently from those in terrestrial counterparts.[62] For example, marinefish gill microbiomes prioritize salt-tolerant bacteria for osmoregulatory support, contrasting with the oxygen-rich, detritus-influenced communities in terrestrial vertebrates.[62]Key examples illustrate these interactions in specific animal systems. Coral holobionts integrate dinoflagellate symbionts like Symbiodinium with bacterial communities, where microbes recycle nutrients and modulate the algal-bacterial interface to sustain photosynthesis and resilience against environmental stress.[63] Bacterial taxa in corals fix nitrogen and produce antimicrobials, fostering stability within the holobiont despite fluctuating conditions.[63] In social insects like bees, the gut microbiota enhances pathogen resistance; core members such as Gilliamella and Snodgrassella inhibit opportunistic invaders like Serratia marcescens through competitive exclusion and antimicrobial production, bolstering colony health.[64] These microbiota-driven defenses are vital for bees, as disruptions increase mortality from bacterial and fungal threats.[64]
Plant Microbiota
Plant microbiota encompass diverse microbial communities associated with above- and below-ground plant tissues, playing crucial roles in nutrient acquisition, growth promotion, and ecological interactions within agricultural and natural ecosystems. These communities are divided into the phyllosphere (aerial parts like leaves), rhizosphere (root-soil interface), and endosphere (internal plant tissues), each hosting specialized microbes that influence plant physiology and environmental adaptation.[65]The phyllosphere, representing the leaf surfaces and aerial structures, is colonized by epiphytic bacteria such as Pseudomonas species, which contribute to nutrient cycling by degrading organic compounds and solubilizing minerals available on leaf surfaces. These bacteria facilitate the recycling of carbon and nitrogen through enzymatic activities that break down leaf exudates and pollutants, enhancing nutrient availability for the host plant and surrounding microbiota. For instance, Pseudomonas strains have been shown to promote phyllospherenitrogen fixation, supporting plant growth in nutrient-limited environments.[66][67]In the rhizosphere, microbial communities interact closely with root exudates, with nitrogen-fixing bacteria like Rhizobium forming symbiotic nodules in legume roots to convert atmospheric nitrogen into ammonia, providing up to 200 kg of fixed nitrogen per hectare annually in optimal conditions. This symbiosis is essential for legume productivity and soil fertility. Complementing this, mycorrhizal fungi, particularly arbuscular mycorrhizal fungi (AMF), extend the root system's reach to improve phosphorus uptake by accessing insoluble soil phosphates through hyphal networks, often contributing 50-80% of a plant's phosphorus needs in phosphorus-poor soils.[68][69]The endosphere harbors intracellular symbionts, including endophytic bacteria, that reside within plant cells and enhance stress tolerance by producing protective compounds such as antioxidants and osmoprotectants, mitigating abiotic stresses like drought and salinity. These symbionts, often from genera like Bacillus and Pseudomonas, modulate host gene expression to maintain cellular homeostasis under adverse conditions.[70][71]Plant growth-promoting rhizobacteria (PGPR), a key subset of rhizosphere and endosphere microbes, enhance crop yields through biofertilizer applications by improving nutrient efficiency and stress resilience, with reported increases of 10-40% in grain and biomass production across various crops. For example, PGPR inoculation in cereals and legumes has boosted yields by facilitating better nitrogen and phosphorus assimilation, reducing reliance on chemical fertilizers.[72][73]
Evolutionary Perspectives
Co-evolution with Hosts
Co-evolution between hosts and their microbiota encompasses reciprocal selective pressures that foster mutual dependencies, with hosts actively selecting beneficial microbes through mechanisms such as immune-mediated partner choice and physiological regulation of colonization sites. For example, hosts deploy antimicrobial peptides and mucus barriers to promote symbionts that enhance nutrient acquisition or immune modulation while excluding pathogens.[74] Concurrently, microbes adapt to host-specific niches by evolving specialized traits, including metabolic pathways tailored to the host's diet and gut anatomy, which in turn reinforce the host's fitness.[75] These adaptations often result in co-speciation patterns, where microbial lineages diverge in parallel with host evolution, though such congruence is more evident in certain taxa than others.[75]Phylogenetic congruence provides compelling evidence for these long-term co-evolutionary processes, as microbial community structures frequently mirror the evolutionary divergence of their hosts. In primates, gut microbiota exhibit phylosymbiosis, with beta-diversity metrics like UniFrac distances showing significant alignment between microbial and host phylogenies across hominids, including humans, chimpanzees, bonobos, and gorillas (P < 0.001).[76] This pattern indicates that co-diversifying microbial lineages, including prokaryotes and phages, have persisted through host speciation events, though signals weaken under environmental perturbations like captivity.[76]Co-evolutionary timescales vary widely across host taxa, reflecting differences in generation times and ecological pressures. In vertebrates, gut microbiota co-evolution with hosts spans millions of years, shaped by phylogenetic history, diet, and morphology to produce clade-specific compositions that enhance host adaptation.[77] By contrast, insects display accelerated dynamics, where microbiome variations drive rapid host genomic adaptation; in Drosophila melanogaster, experimental shifts in microbiota composition alter allele frequencies at hundreds of loci across the genome within five generations (45 days), influencing traits like body mass and population fitness.[78]Central to understanding these interactions is the hologenome theory, which defines the holobiont—the host plus its microbiota—as the fundamental unit of evolution, encompassing the combined genetic material subject to natural selection.[79] Vertical inheritance stabilizes these communities by transmitting core microbial consortia from parent to offspring, often via reproductive tissues or behaviors, thereby maintaining functional consistency and reducing invasion by less adapted strains across generations.[80] This transmission mode enhances the predictability of microbiota assembly and reinforces co-evolutionary stability in diverse host systems.[80]
Genetic Exchange Mechanisms
Horizontal gene transfer (HGT) is a fundamental mechanism driving genetic diversity and adaptation within microbial communities, including host-associated microbiota, by enabling the exchange of genetic material between bacteria outside of vertical inheritance.[81] The primary pathways of HGT—conjugation, transformation, and transduction—facilitate the movement of genes encoding traits such as antibiotic resistance, virulence factors, and metabolic capabilities, significantly influencing microbiota composition and function.[82] In microbial ecosystems like the human gut or environmental biofilms, HGT contributes to 10–20% of protein-coding genes in bacterial genomes, underscoring its role as a major evolutionary force.[82]Conjugation involves direct cell-to-cell contact mediated by conjugative plasmids or integrative conjugative elements (ICEs), allowing the transfer of large DNA segments, often including antibiotic resistance genes.[81] For instance, in the mouse gut, Escherichia coli can transfer plasmids like pTP114 at rates of approximately 0.1 per day, promoting rapid dissemination of resistance determinants among community members.[81] This process is particularly enhanced in biofilms, where close proximity of cells increases conjugation efficiency by up to 1,000-fold compared to planktonic states, with observed rates reaching 2.4 × 10⁻³ transconjugants per recipient per hour under optimal conditions.[83] Transformation, by contrast, entails the uptake of free extracellular DNA by competent cells, a mechanism prevalent in species like Neisseria and Haemophilus, though limited by DNA degradation in complex environments; outer membrane vesicles can protect and deliver DNA, as seen in Klebsiella pneumoniae.[81]Transduction is phage-mediated, where bacteriophages package and transfer bacterial DNA during infection cycles. Generalized transduction occurs when phages erroneously package host DNA, with 1–6% of virions containing such fragments and 10–15% successfully injecting into new hosts, while specialized transduction involves transfer of genes adjacent to prophage integration sites during lysogenic excision.[84] In the human gut microbiota, up to 80% of bacterial genomes harbor prophages, enabling lysogenic cycles that integrate and propagate host genes, such as antibiotic resistance loci in Staphylococcus aureus via autotransduction.[81] These events occur at frequencies of about 1 in 10⁴ virions for specialized transduction, with integration via homologous recombination succeeding in less than 3% of cases in model systems like E. coli with phage P1.[84]The mobilome, comprising mobile genetic elements (MGEs) such as plasmids, transposons, and phages, orchestrates these HGT processes and constitutes a substantial portion of bacterial pangenomes—over 33% in Escherichia—fostering rapid diversification and resilience in microbiota.[81] By shuffling functional gene cassettes, the mobilome not only amplifies trait variability but also supports community-level adaptations, such as metabolic inheritance in infant gut microbiomes through MGE exchange.[81]
Research Approaches
Sequencing-Based Methods
Sequencing-based methods have revolutionized the study of microbiota by enabling high-throughput characterization of community composition without the need for cultivation. Targeted amplicon sequencing focuses on specific genetic markers to profile taxonomic diversity. The most widely used approach for bacteria and archaea involves amplification and sequencing of the 16S ribosomal RNA (rRNA) gene, particularly its hypervariable regions (V1-V9), which provide sufficient variation for distinguishing taxa while conserving universal primer binding sites.[85] For fungi, the internal transcribed spacer (ITS) region, especially ITS1 or ITS2, serves as the standard barcode due to its high interspecies variability and relatively conserved flanking sequences, allowing reliable identification across fungal phyla.[86] However, these PCR-based methods are susceptible to biases, such as preferential amplification of certain taxa due to primer mismatches or GC content differences, which can skew relative abundance estimates and underestimate low-abundance species.In contrast, metagenomic sequencing, often via shotgun approaches, sequences all DNA fragments from a microbial community, providing a culture-independent snapshot of the entire genomic content. This method captures not only bacterial and archaeal genomes but also those of viruses, eukaryotes, and unculturable microbes, yielding data on taxonomic composition through read mapping to reference databases or de novo assembly.[87] Assembly of short reads into contigs remains challenging due to repetitive sequences, uneven coverage, and strain-level heterogeneity, often requiring computational binning to group contigs into metagenome-assembled genomes (MAGs).[88] Binning tools like MetaBAT or CONCOCT address these issues by integrating sequence composition and coverage depth, though they struggle with low-abundance or closely related taxa, leading to fragmented or chimeric bins.[89]Common sequencing platforms influence resolution and cost-effectiveness in microbiota studies. Illumina platforms dominate for short-read sequencing (typically 150-300 bp), offering high throughput and accuracy (>99%) at lower cost, ideal for deep coverage in amplicon or shallow metagenomic surveys. PacBio, using single-molecule real-time sequencing, generates long reads (up to 20 kb) with high fidelity in circular consensus mode (>99.9%), enabling full-length 16S rRNA or better assembly of complex metagenomes, though at higher expense and lower throughput. Oxford Nanopore Technologies (ONT) provides long-read nanopore sequencing with read lengths from thousands to millions of bases, enabling real-time analysis and high-resolution metagenomics, including full-length 16S rRNA for accurate species identification, with recent chemistry achieving >99% accuracy.[90] Post-sequencing, raw data are processed into operational taxonomic units (OTUs) via clustering algorithms at 97% similarity threshold, as implemented in QIIME, or into amplicon sequence variants (ASVs) using error-correction models like DADA2, which resolve fine-scale differences without arbitrary clustering.[85] ASVs provide higher resolution and reproducibility across studies compared to OTUs, reducing artifacts from sequencing errors.[85]Diversity analyses from these datasets quantify microbiota structure using established metrics. Alpha diversity, measuring within-sample richness and evenness, is commonly assessed via the Shannon index, which accounts for both species abundance and rarity (H = -∑ p_i ln p_i, where p_i is the proportion of taxon i), revealing community complexity.[85]Beta diversity, capturing between-sample dissimilarities, employs phylogenetic metrics like UniFrac, which incorporates evolutionary distances on a tree to weight shared branches, distinguishing environmental from neutral turnover in microbiota composition. Weighted UniFrac further integrates relative abundances, enhancing sensitivity to dominant taxa shifts.
Functional and Omics Techniques
Functional and omics techniques provide insights into the active processes and metabolic outputs of microbial communities, complementing taxonomic surveys by revealing gene expression, protein abundance, and metabolite profiles. These approaches, collectively known as meta-omics, enable researchers to study the functional dynamics of microbiota in environments such as the human gut, where microbial activities influence host physiology. By integrating multiple layers of molecular data, these methods uncover pathways that drive community behavior, such as nutrient cycling and host-microbe interactions.[91]Metatranscriptomics employs RNA sequencing (RNA-seq) to capture the transcriptome of microbial communities, quantifying active gene expression and identifying functional pathways without relying on reference genomes. This technique sequences total RNA from samples, often after rRNA depletion, to profile mRNA transcripts and reveal which genes are transcribed under specific conditions, such as in the gut microbiota during dietary shifts. For instance, metatranscriptomic analyses have shown upregulated carbohydrate metabolism pathways in human gut communities responding to fiber-rich diets, highlighting active microbial roles in fermentation. Key challenges include distinguishing host from microbial RNA and handling low-abundance transcripts, but advancements in long-read sequencing have improved resolution of operons and regulatory elements. Seminal work demonstrated that metatranscriptomes correlate with metagenomes but reveal dynamic expression patterns, such as diurnal shifts in oral microbiota metabolism during health and disease.[92][91][93]Metaproteomics uses mass spectrometry to detect and quantify proteins directly from complex samples, providing a snapshot of the functional proteome and enzymatic activities within microbiota. Liquid chromatography coupled with tandem mass spectrometry (LC-MS/MS) is the primary method, fragmenting peptides for identification via database searching against predicted microbial proteomes. In gut microbiota studies, metaproteomics has identified enzymes involved in bile acid transformation, such as bile salt hydrolases from Firmicutes species, linking protein abundance to metabolic outputs like short-chain fatty acid production. This approach bridges the gap between potential (genomic) and realized (expressed) functions, though it faces hurdles like low protein recovery from environmental samples and host protein interference. High-impact research has mapped metaproteomic profiles in fecal samples, revealing conserved functional modules across individuals despite taxonomic variability.[94][95][96]Metabolomics profiles small molecules produced or modified by microbiota, using techniques like nuclear magnetic resonance (NMR) spectroscopy or mass spectrometry (MS) to detect metabolites such as short-chain fatty acids (SCFAs) in host-associated niches. Untargeted metabolomics surveys the entire metabolome for discovery, while targeted approaches quantify specific compounds like butyrate, a SCFA derived from gut microbial fermentation of dietary fibers. In microbiota research, these methods have elucidated how Bacteroides species contribute to propionate production, influencing host energy homeostasis. NMR offers structural insights without derivatization, whereas MS provides higher sensitivity for low-abundance metabolites, though both require careful sample preparation to avoid contamination. Reviews emphasize metabolomics' role in linking microbial consortia to phenotypic effects, such as anti-inflammatory SCFAs in the colon.[97][98][99]Multi-omics integration combines data from metatranscriptomics, metaproteomics, and metabolomics to model holistic microbial functions, using computational frameworks like network analysis or machine learning to correlate layers. This approach reveals regulatory relationships, such as how transcript levels predict protein outputs and metabolite fluxes in gut communities. For example, integrated analyses have shown coordinated upregulation of amino acid degradation pathways across omics in response to protein-rich diets. Tools like DIABLO or mixOmics facilitate statistical integration, accounting for data sparsity and batch effects. High-impact studies demonstrate that multi-omics enhances predictive power for community resilience compared to single-omics alone.[100][101][102]Recent advances include spatial omics techniques that combine multi-omics with spatial profiling to visualize microbial distributions and activities in situ. For instance, Microbiome Cartography (MicroCart) enables simultaneous assessment of host and microbiome across modalities like transcriptomics and imaging, revealing spatially resolved interactions in gut and tumor environments as of 2025.[103]Flux balance analysis (FBA) is a constraint-based modeling technique that predicts metabolic fluxes in microbial communities by optimizing biomassproduction under stoichiometric constraints, often integrated with omics data for microbiota studies. Genome-scale metabolic models (GEMs) are reconstructed from metagenomic annotations, then FBA simulates steady-state fluxes to infer interactions like cross-feeding in gut consortia. Applications include modeling SCFA production by Clostridium species, where FBA quantifies how nutrient availability directs communitymetabolism. This method assumes quasi-steady state and maximizes growth, validated against experimental fluxes in simplified communities. Reviews highlight FBA's utility in predicting host-microbe metabolic exchanges, such as vitaminsynthesis dependencies.[104][105][106]
Key Research Initiatives
Major International Projects
The Human Microbiome Project (HMP), launched by the National Institutes of Health (NIH) in 2007 and concluding its primary phase in 2013, aimed to characterize microbial communities across the human body and their roles in health and disease.[107] This initiative sequenced approximately 3,000 reference bacterial genomes from human-associated microbes, providing a foundational catalog for subsequent research.[107] In its second phase, known as the Integrative Human Microbiome Project (iHMP) from 2014 to 2016, the effort shifted to longitudinal studies, examining dynamic changes in microbiota over time in relation to host conditions such as pregnancy, inflammatory bowel disease, and prediabetes.[108]The Earth Microbiome Project (EMP), initiated in 2010 and ongoing, seeks to create a global reference database of microbial diversity across environmental biomes through crowd-sourced sampling and standardized sequencing protocols.[109] As of 2017, the project has analyzed over 27,000 samples from diverse habitats worldwide, with plans to expand to 200,000 samples to map microbial patterns at an unprecedented scale.[110] These efforts have revealed multiscale microbial diversity, including bacterial and archaeal communities, contributing to understandings of ecological roles in terrestrial, aquatic, and atmospheric systems.[111]The MetaHIT consortium, funded by the European Commission from 2008 to 2013, focused on metagenomics of the human intestinal tract to elucidate gut microbiota composition in health and disease across European populations.[112] Involving 15 institutes from eight countries, MetaHIT generated a catalog of 3.3 million non-redundant microbial genes from fecal samples of over 120 individuals, identifying key functional pathways and enterotypes associated with metabolic conditions.[113]These projects have collectively advanced microbiota research by establishing public databases such as MG-RAST, an open-source platform for metagenomic analysis that has processed millions of sequences since 2008, facilitating data sharing and comparative studies.[114] Additionally, they developed standardization protocols for sampling, sequencing, and metadata reporting, enabling interoperability across global initiatives and reducing variability in microbiota datasets.[115]
Collaborative Databases and Repositories
Collaborative databases and repositories are essential open-access platforms that facilitate the storage, standardized analysis, and global sharing of microbiota data, enabling researchers to integrate diverse datasets for comparative studies and hypothesis generation. These resources emphasize reproducibility through versioned pipelines and interoperable formats, supporting advancements in understanding microbial communities across hosts and environments.[116]QIIME 2 serves as a widely adopted workflow for processing amplicon data, such as 16S rRNA gene sequences commonly used in microbiota surveys. It provides a modular, plugin-based framework for denoising raw reads, performing taxonomic assignment via classifiers like SILVA or Greengenes, and computing alpha and beta diversity metrics. The platform includes visualization tools, such as the QIIME 2 View interface, which generates interactive graphics for exploring community composition and statistical results, enhancing accessibility for both novice and expert users.[117]MGnify, hosted by the European Molecular Biology Laboratory's European Bioinformatics Institute (EMBL-EBI), functions as a comprehensive metagenomic analysis pipeline and repository for raw and processed microbiome sequences. It automates taxonomic profiling using tools like MetaPhlAn and functional annotation via eggNOG-mapper, handling over 500,000 public datasets that span amplicon, metagenomic, and metatranscriptomic data types. This resource supports large-scale submissions and re-analysis, promoting data reuse through its browser-based exploration features.[118][116]The Human Microbiome Project (HMP) Data Portal integrates datasets from the NIH-funded HMP's two phases, offering centralized access to metagenomic, metatranscriptomic, and 16S rRNA profiles from thousands of human samples across body sites like the gut, skin, and oral cavity. It includes processed data such as gene catalogs and pathway abundances, derived from over 20,000 samples, to support investigations into microbiota-host interactions. The portal's search tools allow querying by metadata like health status or site, streamlining multi-omics integration.[119][120]A hallmark of these repositories is their adherence to annotation standards, exemplified by integration with KEGG pathways to map microbial functions such as carbohydrate metabolism and virulence factors, providing insights into community capabilities without exhaustive manual curation. Interoperability is enhanced through compatibility with the NCBI Sequence Read Archive (SRA), where raw reads are deposited and linked, allowing seamless data retrieval and cross-platform analyses via APIs and standardized ontologies.[116]
Health and Ecological Implications
Role in Host Health and Disease
The gut microbiota contributes significantly to host health by fortifying the intestinal barrier function, primarily through the production of short-chain fatty acids (SCFAs) that nourish colonic epithelial cells and enhance the thickness and integrity of the protective mucus layer.[121] Specific taxa, such as Akkermansia muciniphila, further support this barrier by promoting mucin production and preventing pathogen adhesion to the epithelium.[122] Additionally, certain microbiota members synthesize essential vitamins unavailable or insufficiently produced by the host, including vitamin K, which is critical for blood coagulation, and vitamin B12, necessary for red blood cell formation and neurological health.[123] These functions collectively aid in nutrient metabolism, pathogen resistance, and overall physiological homeostasis.[124]Dysbiosis, marked by reduced microbial diversity and shifts in composition, is strongly associated with various host diseases. In inflammatory bowel disease (IBD), patients exhibit a notable decrease in the Firmicutes phylum, alongside increased Proteobacteria, which correlates with heightened inflammation and barrier dysfunction.[125] For type 2 diabetes, depletion of butyrate-producing bacteria, such as those in the Faecalibacterium and Roseburia genera, results in butyrate deficiency, impairing gut integrity, insulin signaling, and glucose homeostasis.[126] In colorectal cancer, enrichment of Fusobacterium nucleatum in tumor tissues promotes oncogenesis by inducing tumor cell proliferation and immune evasion through mechanisms like Wnt/β-catenin pathway activation.[127] These alterations underscore the microbiota's role in transitioning from health to pathology.Microbiota-host interactions occur through key mechanisms that modulate immunity and metabolism. The microbiota stimulates inflammasome activation in host immune cells, such as NLRP6 and NLRP3 complexes, which release interleukin-18 to reinforce epithelial barrier integrity and combat pathogens, though excessive activation can drive chronic inflammation in dysbiotic states.[128] Metabolite signaling further links microbiota to disease; for instance, microbial conversion of dietary nutrients like choline into trimethylamine N-oxide (TMAO) in the liver promotes foam cell formation and atherosclerosis, elevating cardiovascular disease risk.[129] These pathways highlight the microbiota's bidirectional influence on host physiology.Therapeutic interventions targeting microbiota restoration have demonstrated clinical promise. Fecal microbiota transplantation (FMT) achieves approximately 90% success in resolving recurrent Clostridioides difficile infections by replenishing beneficial taxa and suppressing pathogen overgrowth.[130] Post-2020 research on COVID-19 has shown that SARS-CoV-2 infection induces gut dysbiosis, with reduced microbial diversity and enrichment of opportunistic pathogens correlating to disease severity and prolonged symptoms.[131]
Environmental and Agricultural Impacts
Microbiota play crucial roles in environmental ecosystems by facilitating nutrient cycling, which sustains soil fertility and plant productivity. In terrestrial environments, soil microbiota, including bacteria and fungi, drive the decomposition of organic matter and the mineralization of essential nutrients such as nitrogen, phosphorus, and potassium. For instance, actinomycetes, a group of filamentous bacteria including genera like Streptomyces and Actinomyces, contribute to nitrogen cycling by enhancing the availability of fixed nitrogen through symbiotic associations and organic matter breakdown, thereby supporting soil ecosystem stability. In aquatic systems, marine microbiota are integral to the microbial carbon pump, where heterotrophic bacteria convert labile organic carbon into recalcitrant dissolved organic matter, promoting long-term carbon sequestration in ocean depths and mitigating atmospheric CO₂ levels. This process accounts for a significant portion of the ocean's capacity to store 5-10 gigatons of carbon annually, underscoring the microbiota's influence on global carbon fluxes.In agriculture, microbiota serve as biofertilizers and biocontrol agents, reducing reliance on chemical inputs while boosting crop yields. Bacteria such as Azospirillum brasilense form associations with plant roots, particularly in cereals like maize, where inoculation has been shown to increase grain yield by approximately 5.4% on average through enhanced nitrogen uptake and root growth promotion. Similarly, soil microbiota contribute to phytopathogen control by outcompeting harmful microbes, producing antimicrobial compounds, or inducing plant systemic resistance; for example, beneficial rhizosphere communities suppress pathogens like Ralstonia solanacearum in crops, leading to reduced disease incidence and improved agricultural sustainability.Microbiota also enable bioremediation, the degradation of environmental pollutants, with species like Pseudomonas aeruginosa and Pseudomonas putida playing key roles in breaking down hydrocarbons in oil spills. These bacteria utilize crude oil as a carbon source, achieving substantial degradation rates—up to 70-80% of saturates and aromatics in contaminated sites—through enzymatic pathways that mineralize toxic compounds into harmless byproducts. Advances in microbiome engineering further amplify these applications by designing synthetic microbial communities (SynComs), which integrate keystone species to enhance pollutant breakdown or nutrient cycling in targeted environments. However, climate change poses challenges to these functions, as rising temperatures and altered precipitation patterns reduce soil microbiota diversity; long-term warming experiments indicate declines in microbial α-diversity by 10-20%, shifting community composition toward stress-tolerant taxa like Firmicutes while diminishing metabolic versatility essential for ecosystem resilience.
Contemporary Challenges
Effects of Perturbations like Antibiotics
Antibiotics, particularly broad-spectrum ones, disrupt the gut microbiota by indiscriminately targeting bacterial populations, leading to a reduction in microbial diversity and the proliferation of resistant strains. This perturbation, known as dysbiosis, alters the balance of beneficial and pathogenic microbes, compromising the microbiota's protective functions. For instance, broad-spectrum antibiotics like cephalosporins and fluoroquinolones can decrease overall bacterial richness by 25-50%, while selectively favoring the survival of opportunistic pathogens.[132]A classic example is amoxicillin, a commonly prescribed beta-lactamantibiotic, which significantly reduces populations of beneficial genera such as Bifidobacterium in both children and adults. In pediatric studies, amoxicillin treatment has been shown to decrease Bifidobacterium spp. relative abundance while increasing Prevotella spp., persisting for weeks post-treatment. This selective depletion weakens colonization resistance, the microbiota's ability to inhibit pathogen invasion, and can extend to long-term compositional shifts even after a single course.[133][134]The consequences of such disruptions include heightened susceptibility to infections, notably overgrowth of Clostridioides difficile, which thrives in the altered environment depleted of competing microbes. Antibiotic exposure is the primary risk factor for C. difficile infection, with broad-spectrum agents like clindamycin and cephalosporins elevating odds by disrupting microbiota barriers, leading to severe diarrhea and colitis in up to 20% of hospitalized cases. Additionally, early-life antibiotic exposure has been linked to increased obesity risk through microbiota-mediated metabolic changes, with cohort studies showing a dose-dependent association where multiple courses before age 2 correlate with higher body mass index in childhood due to reduced microbial diversity and altered energy harvest from diet.[135][136][137]Recovery from antibiotic-induced dysbiosis is often partial and protracted, with the microbiota exhibiting resilience but rarely returning to pre-treatment composition fully. In healthy adults, bacterial diversity may rebound to near-baseline levels within 1.5 months, yet certain species remain absent for years, and full functional restoration can take up to two years in some cases. Probiotics, such as strains of Lactobacillus and Bifidobacterium, can mitigate these effects by accelerating recolonization and preserving diversity during and after treatment, though their efficacy varies by individual microbiota baseline and antibiotic type.[138][139]Studies from the 2020s have highlighted the proliferation of the antibiotic resistome—the collection of resistance genes within the microbiota—following exposure, with antibiotics like amoxicillin enriching antimicrobial resistance genes (ARGs) in gut communities, potentially disseminating them horizontally to pathogens. This expansion, observed in both human and animal models, underscores the role of antibiotics in accelerating global resistance, with ARG abundance increasing up to 10-fold post-treatment in some cohorts. As of 2024, the World Health Organization reported only 12 new antibacterial agents in clinical development, emphasizing ongoing challenges in combating resistance amid persistent microbiota disruptions.[140][141]Beyond antibiotics, non-antibiotic perturbations such as dietary shifts and environmental pollution also induce microbiota alterations with lasting impacts. High-fat, low-fiber Western diets reduce beneficial taxa like Bifidobacterium and Eubacterium, promoting inflammation and metabolic dysfunction similar to antibiotic effects. Pollutants, including heavy metals and microplastics ingested via diet or water, disrupt microbial composition by favoring toxin-resistant strains and impairing biotransformation, thereby elevating host exposure to harmful compounds. Recent 2025 studies have further shown microplastics significantly alter gut microbiota diversity and metabolite profiles, with between-group distances 87.75% higher than controls.[142][143][144]
Ethical and Privacy Concerns
Microbiota research generates vast amounts of genomic data that pose significant privacy risks due to the potential for re-identification of individuals, even from anonymized datasets. Unlike traditional genetic data, microbiome profiles exhibit unique temporal and site-specific stability, enabling attackers to link samples back to donors through microbial composition patterns. A foundational 2015 study using data from the Human Microbiome Project demonstrated that gut microbiome profiles, derived from both 16S rRNA amplicon sequencing and shotgun metagenomics, could uniquely identify individuals among a cohort of 242 with greater than 80% accuracy, highlighting the traceability of such data across body sites. Subsequent analyses have confirmed these risks extend to aggregated summary statistics, where re-identification success rates show high power with type II error probabilities far less than 0.01 in controlled small-scale datasets of human-associated microbial abundances, underscoring the inadequacy of current de-identification methods for microbiota information.[145][146]Ethical challenges in microbiota research are amplified by the intricacies of informed consent for sampling and data use, given the unpredictable future applications of microbiome profiles in diagnostics, therapeutics, and forensics. Participants may not fully comprehend the perpetual nature of microbial data or its potential to reveal sensitive health inferences, such as disease predispositions, necessitating dynamic consent models that allow ongoing oversight. Bioprospecting efforts targeting diverse microbial communities in indigenous populations further complicate ethics, as historical precedents of resource extraction without equitable benefit-sharing have led to exploitation concerns; for instance, research involving Amazonian or Arctic communities has prompted calls for community veto rights and co-ownership of derived intellectual property to prevent neocolonial dynamics. These issues are particularly acute in global collaborations, where power imbalances between researchers and participants can undermine trust. In 2025, a Yanomami framework advanced ethical Indigenous microbiome research, advocating dedicated funding for community initiatives, sustained oversight, and benefit-sharing.[147][148][149]Equity in microbiota research remains a pressing concern, with major databases heavily skewed toward Western populations, limiting the generalizability of findings and exacerbating health disparities. Public repositories, such as those aggregating over 220,000 human microbiome samples, show that sub-Saharan African contributions represent only 1.3% of the total, despite the region housing 14% of the global population and harboring potentially unique microbial diversity influenced by local diets and environments. The Human Microbiome Project, a landmark initiative, exemplifies this bias, predominantly featuring North American participants with limited representation from non-Western ancestries outside the U.S., including minimal African representation, which hinders insights into microbiota variations relevant to tropical diseases prevalent in underrepresented regions. Efforts to address this include targeted sampling in diverse cohorts, but persistent underfunding and logistical barriers in low-resource settings perpetuate the gap. A 2025 study expanded the African gut microbiome atlas, identifying over 40,000 previously unknown microbes and providing a framework for equitable global research.[150][151]Key developments in mitigating these concerns include the application of the General Data Protection Regulation (GDPR) since 2018, which classifies microbiota data as personal health information when re-identifiable, mandating explicit consent, data minimization, and rights to erasure for EU-involved research. This has spurred the development of privacy-preserving techniques, such as federated learning for microbiome analyses without centralizing raw data. Complementing this, international calls for ethical open-access practices have intensified; for example, 2022 guiding principles emphasize community engagement, benefit-sharing, and inclusive governance in microbiome repositories to balance data sharing with protections, influencing policies in projects like the Earth Microbiome Project. These frameworks aim to foster equitable, responsible advancement while safeguarding vulnerable groups.[152][148]