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Nanobdellati

Nanobdellati is a kingdom of archaea distinguished by its members' ultra-small cell sizes, typically in the nanometer range, and highly reduced genomes that encode limited metabolic pathways.^[1] These organisms, previously grouped under the DPANN superphylum, often rely on symbiotic or parasitic interactions with host prokaryotes for survival, reflecting their dependence on external nutrient sources and reduced biosynthetic capacities.^[2] The kingdom encompasses several phyla, including Nanoarchaeota, Micrarchaeota, Aenigmatarchaeota, Iainarchaeota, Nanohaloarchaeota, Parvarchaeota, Diapherarchaeota, Pacearchaeota, and Woesearchaeota, and is defined by phylogenetic analyses of single-amplified genomes from diverse environments such as marine sediments, hydrothermal vents, and subsurface aquifers.^[1]^[3] Formally proposed as a taxonomic rank in 2024, Nanobdellati derives its name from the type genus Nanobdella, a thermoacidophilic, obligate ectosymbiotic archaeon isolated from hot springs.^[4] Etymologically, "Nanobdellati" combines the neuter noun Nanobdella with the suffix "-ati" to denote a kingdom, highlighting the group's leech-like (bdella meaning leech in Greek) attachment to hosts in many cases.^[4] Genomic studies reveal notable features such as bacterial-like sigma factors for transcription and evidence of extensive horizontal gene transfer, including eukaryotic-derived genes, which contribute to their unique coding potential.^[1] These traits underscore Nanobdellati's evolutionary distinctiveness within Archaea, positioning them as a key group for understanding microbial symbiosis and genome reduction.^[5] Nanobdellati archaea are ubiquitous in microbial communities worldwide, detected through metagenomics in habitats ranging from hypersaline waters to deep biosphere settings, yet few have been cultured due to their obligate host dependence.^[6] Recent advances, including cryo-electron tomography, have illuminated their intimate cell-to-cell interactions, such as adhesion structures that facilitate nutrient exchange with hosts.^[7] Biochemical insights, like autonomous N-linked protein glycosylation using host-derived substrates, further highlight their adapted biology despite genomic minimalism.^[8] As of 2025, new lineages such as Candidatus Sukunaarchaeum mirabile have been described, featuring one of the smallest known archaeal genomes and extreme metabolic reduction.^[9] As research progresses, Nanobdellati continues to challenge traditional views of archaeal diversity and independence, offering windows into ancient microbial evolution.

History and Discovery

Initial Identification

The initial identification of the DPANN archaea, later encompassing the group now known as Nanobdellati, stemmed from metagenomic surveys of groundwater and acidic environments conducted in 2013. Researchers analyzed single amplified genomes (SAGs) from diverse sites, including aquifer sediments and acid mine drainage biofilms, revealing novel archaeal lineages with 16S rRNA gene sequences that branched deeply within the archaeal domain. These included phyla such as Parvarchaeota (formerly ARMAN), Aenigmarchaeota, Diapherotrites, Nanoarchaeota, and Nanohaloarchaeota, collectively forming a monophyletic radiation characterized by ultrasmall cell sizes and genome sizes often below 1 Mb. Early characterizations highlighted extensive genome reduction in these archaea, with many lacking key biosynthetic pathways for amino acids, nucleotides, and cofactors, suggesting a lifestyle dependent on host interactions. For instance, Nanoarchaeum equitans, the first described member of Nanoarchaeota from a hydrothermal vent, exhibited a highly reduced genome of approximately 490 kb and was observed as an ectosymbiont on Ignicoccus hospitalis, relying on its host for metabolic support. Metagenomic reconstructions further indicated divergence from other archaea through widespread gene loss, alongside evidence of horizontal gene transfer (HGT) from bacteria—such as genes for fatty acid biosynthesis—and potentially from eukaryotes, enabling adaptations like membrane lipid modifications. These findings positioned DPANN as a distinct archaeal superphylum with potential parasitic or symbiotic ecologies. The first cultured representative beyond N. equitans, Nanopusillus acidilobi (a Nanoarchaeota species), was isolated in 2016 from an acidic hot spring in Yellowstone National Park using genomics-informed co-culture with its host, Sulfolobus acidocaldarius. This achievement confirmed the symbiotic nature of these interactions, as N. acidilobi cells (100–300 nm in diameter) attached to host cells and displayed limited metabolic capabilities, including partial glycolysis and reliance on host-derived metabolites. Such cultivation efforts validated initial hypotheses from metagenomic data, underscoring the parasitic tendencies inferred from genomic streamlining.

Recent Reclassification

In 2024, Rinke et al. proposed elevating the diverse group of archaea previously known as the DPANN superphylum to the rank of kingdom, designated as Nanobdellati (regn. nov.), within the domain Archaea.^[4] This reclassification was formally validated by Göker and Oren, reflecting advancements in phylogenomic analyses that justified the higher taxonomic status.^[4] The name Nanobdellati derives from the type genus Nanobdella (Kato et al. 2022), which combines the Greek words nanos (dwarf) and bdella (leech), alluding to the small size and leech-like parasitic attachment of these organisms to their hosts.^[10]^[4] The rationale for this reclassification stems from genomic and phylogenetic evidence demonstrating a deep, isolated branching position of these archaea within the archaeal domain, distinct from other major lineages such as Methanobacteriati and Thermoproteati.^[4] Extensive genome reduction, with many members possessing ultrasmall genomes ranging from 0.49 to 1.2 Mb, underscores their unique evolutionary trajectory, often involving dependency on host organisms for metabolic functions.^[11]^[4] This separation highlights a long, independent history marked by adaptations to symbiotic or parasitic lifestyles, setting Nanobdellati apart from the more metabolically versatile archaeal phyla.^[4] Nomenclatural updates accompanying the proposal integrate the former DPANN acronym—encompassing the phyla Diapherotrites, Parvarchaeota, Aenigmarchaeota, Nanoarchaeota, and Nanohaloarchaeota—into the new kingdom framework, while incorporating additional lineages such as Micrarchaeota (Sakai et al. 2023).^[11]^[4] Other phyla now included are Huberarchaeota and Iainarchaeota, expanding the kingdom to reflect the growing diversity revealed by metagenomic surveys and single-cell sequencing.^[4] This restructuring aligns with the Genome Taxonomy Database (GTDB) classifications and emphasizes the monophyletic nature of Nanobdellati based on average nucleotide identity and phylogenetic trees.

Morphology and Cellular Features

Ultrasmall Size and Structure

Nanobdellati exhibit ultrasmall cell dimensions, typically ranging from 100 to 500 nm in diameter, positioning them among the smallest free-living cellular organisms known.^[12] This nanoscale size confers a high surface area-to-volume ratio, which supports efficient nutrient diffusion and uptake across the cell membrane despite their limited metabolic capabilities.^[13] For instance, cells of Nanoarchaeum equitans are spherical and measure approximately 400 nm in diameter, while those of Nanobdella aerobiophila are coccoid with diameters of 200–500 nm.^[14] Electron microscopy reveals distinctive cellular structures adapted to their diminutive scale, including minimal ribosome numbers—often around 92 per cell in some lineages—and reduced organelle-like features.^[15] These ribosomes, visualized in ultrastructural studies, are compact to fit within the constrained cytoplasmic volume. Some Nanobdellati lack canonical archaeal surface features, such as S-layers homologous to those in other archaea, though others possess thin, proteinaceous S-layers (15–20 nm thick) with oblique lattice arrangements and no detectable pseudomurein in their cell walls.^[16] Cryo-electron tomography of Nanobdella aerobiophila highlights a cytoplasmic membrane (3–4 nm thick) punctuated by ~30 nm pores, potentially allowing passage of small molecules or even ribosomes.^[17] Recent cryo-electron tomography has further revealed a conical attachment organelle at the host interface, consisting of concentric arrays of short cylindrical shells that may facilitate adhesion.^[18] Notable morphological variations include attachments of icosahedral virus-like particles in certain members, as observed in Nanopusillus acidilobi, where these ~65 nm particles associate with the host-parasite interface via transmission electron microscopy.^[19] Such structures underscore the phylum's structural simplicity, correlating with their reduced genome sizes that limit complexity in cellular components.^[20]

Genome Reduction and Metabolic Traits

Nanobdellati exhibit highly reduced genomes, typically ranging from 0.5 to 1.5 Mb in size, a feature that underscores their adaptation to a parasitic lifestyle with profound metabolic dependencies on host organisms.^[21]^[22] This genome streamlining involves extreme gene reduction, with the loss of entire pathways essential for independent metabolism, including glycolysis, the tricarboxylic acid (TCA) cycle, and de novo nucleotide synthesis, compelling these archaea to scavenge nucleotides, amino acids, lipids, and other biomolecules directly from their hosts.^[22]^[23] For instance, the model organism Nanoarchaeum equitans possesses a 0.49 Mb genome encoding only about 552 protein-coding genes, devoid of capabilities for ATP production or lipid biosynthesis, highlighting the minimalistic genetic repertoire that prioritizes replication over autotrophic functions.^[22] Horizontal gene transfer (HGT) has played a role in shaping Nanobdellati genomes, enabling the acquisition of genes that support host interactions despite overall reduction; notable examples include transfers from bacterial donors for membrane-associated functions and eukaryotic-like proteins that may aid in cellular processes, though biosynthetic pathways remain severely limited and reliant on host scavenging.^[22] Their translation machinery is correspondingly pared down, featuring fewer tRNA genes—often as low as 35–38 functional species in lineages like Nanoarchaeota—some of which are uniquely split into 5' and 3' halves that require trans-splicing for maturation, reflecting evolutionary pressures to conserve genomic space.^[22] Additionally, Nanobdellati genomes consistently lack genes for flagellar biosynthesis, consistent with their sessile, host-attached lifestyle and absence of motility.^[22]^[13] Recent investigations have uncovered specialized metabolic traits that enhance host dependency while allowing limited autonomy, such as the capacity for N-linked protein glycosylation in cultivated species like Nanobdella aerobiophila. A 2024 study revealed that this archaeon encodes a complete glycosylation machinery, including the oligosaccharyltransferase homolog aglB, enabling autonomous assembly of complex glycans (e.g., Hex₄HexNAc₂) using host-derived sugar substrates scavenged via adhesion mechanisms, which likely facilitates host recognition and symbiotic stability without independent sugar biosynthesis.^[24] These traits exemplify how Nanobdellati balance genomic minimalism with targeted adaptations, ensuring survival through intimate host parasitism rather than broad metabolic versatility.^[24]

Ecology and Interactions

Environmental Distribution

Nanobdellati, formerly known as DPANN archaea, predominate in extreme environments such as acidic hot springs, deep subsurface aquifers, and marine sediments. In Yellowstone National Park's geothermal features, lineages like Nanoarchaeota thrive in acidic (pH ~2) and high-temperature (up to 75°C) conditions, as evidenced by metagenomic surveys of sites including Crater Hills and Nymph Lake.^[19] Similarly, they are abundant in deep terrestrial subsurface aquifers, such as those in the Colorado Plateau, where they form symbiotic associations in anoxic, oligotrophic groundwater ecosystems.^[25] In marine settings, Nanobdellati inhabit oxygen-deficient zones (ODZs) and underlying sediments in regions like the Eastern Tropical Pacific and Arabian Sea, contributing to anoxic microbial communities.^[26] They are notably rare in mesophilic soils, where their detection is infrequent compared to aquatic or subsurface habitats.^[27] Detection of Nanobdellati primarily occurs through 16S rRNA gene amplicon sequencing and metagenomics, enabling identification in diverse biomes without cultivation. These methods have revealed their presence across global samples, including hydrothermal vents and thawed permafrost.^[28] Abundance varies by habitat; in some groundwater aquifers, they constitute 10-24% of the archaeal community, particularly in contaminated sites, while in pristine aquifers, they comprise less than 5%.^[3] In ODZ water columns, they can reach up to 1% of the total microbial community and 25-50% of archaea at anoxic depths around 200 m.^[26] In hot springs, however, their relative abundance is lower, often around 0.1% of cellular reads.^[19] Biogeographic patterns show higher diversity in geothermal sites, such as hydrothermal vents, where uncultured lineages dominate the archaeal assemblages. For instance, Parvarchaeota and related groups are prevalent in deep-sea vent sediments, comprising a significant portion of recovered metagenome-assembled genomes.^[29] This elevated diversity in thermal environments contrasts with more uniform distributions in subsurface aquifers, underscoring their adaptation to geochemically extreme niches.^[28]

Symbiotic and Parasitic Relationships

Nanobdellati exhibit obligate symbiotic relationships with other archaea, relying on direct physical attachment to their hosts for survival and growth. A well-studied example is Nanoarchaeum equitans, which adheres to the surface of its host Ignicoccus hospitalis using pili-like structures derived from a type IV protein export system, facilitating stable cocultivation in hydrothermal environments.^[30]^[31] These attachments enable the transfer of essential nutrients, as N. equitans lacks many biosynthetic pathways and depends on host-derived compounds.^[32] The interactions display parasitic traits, with Nanobdellati extracting nutrients such as amino acids from hosts, often resulting in inhibited host cell proliferation and reduced growth rates.^[33] Recent cryo-electron tomography analyses of the Nanobdellati Nanobdella aerobiophila and its host Metallosphaera sedula reveal intimate membrane contacts via a conical attachment organelle composed of concentric cylindrical shells, allowing close association without host cell lysis.^[34] This structure supports nutrient exchange while preserving host integrity, highlighting a non-destructive parasitic strategy.^[35] Evolutionarily, Nanobdellati serve as models for early archaeal diversification due to their reduced genomes and extensive horizontal gene transfer (HGT) from hosts, which aids adaptation to symbiotic lifestyles. For instance, glycosylation pathways in Nanobdellati enable autonomous glycan synthesis for protein modifications, utilizing substrates derived from host metabolism to support cell surface structures critical for attachment.^[24] Such HGT events, including those involving membrane and metabolic genes, underscore their role in archaeal evolutionary history.^[30]

Classification and Phylogeny

Taxonomic Hierarchy

The kingdom Nanobdellati was formally established in 2024 as part of a revised classification of Archaea, encompassing ultrasmall archaea previously grouped under the informal DPANN superphylum.^[4] This kingdom is positioned within the domain Archaea and includes several phyla characterized by reduced genomes and symbiotic lifestyles.^[4] The nomenclature follows the International Code of Nomenclature of Prokaryotes (ICNP), with validly published names tracked by the List of Prokaryotic names with Standing in Nomenclature (LPSN).^[36] The type genus is Nanobdella, with the type species Nanobdella aerobiophila, derived from etymologies reflecting small size ("nano-") and leech-like symbiosis ("bdella").^[37] The primary phyla under Nanobdellati are Aenigmarchaeota, Diapherotrites, Micrarchaeota, Nanoarchaeota, Nanohaloarchaeota, and Parvarchaeota, all designated as Candidatus due to their uncultured status at the time of proposal, though some lower taxa have valid names.^[4] Nanoarchaeota, for instance, includes the validly published class Nanoarchaeia, order Nanoarchaeales, family Nanoarchaeaceae, and genus Nanoarchaeum, with type species Nanoarchaeum equitans (etymology: "equitans," riding, referring to its attachment to host cells). Micrarchaeota encompasses genera like Nanopusillus, with type species Candidatus Nanopusillus acidilobi (etymology: "acidilobi," acid-loving, adapted to acidic hot springs). In Nanohaloarchaeota, the type genus is Candidatus Nanohaloarchaeum, exemplified by Candidatus Nanohaloarchaeum antarcticus (etymology: "nanohaloarchaeum," small salt-loving archaeon), representing halophilic members associated with hypersaline environments. Nomenclature updates in 2024 validated the kingdom-level name while retaining Candidatus status for most phyla to reflect ongoing cultivation challenges, with LPSN listing 17 child taxa including additional lineages like Pacearchaeota.^[36] Key genera such as Nanoarchaeum (thermophilic symbionts of Ignicoccus hosts) and Candidatus Nanopusillus (acidic epibionts) highlight the kingdom's diversity in extremophilic niches.

Phylogenetic Position

Nanobdellati are often positioned as a basal group within the archaeal domain, emerging as a deeply branching monophyletic clade in multi-gene phylogenomic analyses that suggest them as an early-diverging sister to all other Archaea.^[38]^[39]^[40] This placement distinguishes them from the TACK superphylum (Thaumarchaeota, Aigarchaeota, Crenarchaeota, and Korarchaeota), with their unique evolutionary trajectory shaped by extreme genome streamlining and reductive adaptations, resulting in ultrasmall genomes averaging around 0.6-1.0 Mbp. Recent studies, including those from 2020 onward, support this topology through increased taxon sampling and advanced phylogenetic models that account for compositional heterogeneity, though the position remains debated.^[38]^[39] Recent 2025 studies have identified additional lineages, such as Sukunaarchaeum, further expanding the known diversity within Nanobdellati.^[9] Genomic investigations highlight extensive horizontal gene transfer (HGT) as a key driver of Nanobdellati evolution, with significant acquisition of genes from bacterial sources, including CRISPR-Cas systems such as the subtype II-D variants prevalent in nanoarchaeal lineages. These transfers, often comprising a notable proportion of their reduced gene repertoires, facilitate adaptations like defense mechanisms and metabolic supplementation, while inter-clade exchanges with archaeal hosts further indicate a reticulate evolutionary pattern rather than strict vertical inheritance. Such HGT events are particularly evident in symbiotic contexts, underscoring the role of ecological interactions in shaping their genomes.^[41]^[39] The monophyly of Nanobdellati has been debated, with some analyses suggesting potential paraphyly arising from phylogenetic artifacts like long-branch attraction (LBA), exacerbated by their accelerated substitution rates and gene loss. However, refined methodologies, including site-heterogeneous models and broader genomic datasets, have largely resolved these issues, affirming their unity as a distinct basal archaeal radiation while highlighting the challenges of reconstructing deep evolutionary relationships in streamlined lineages.^[42]^[38]

References

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### Description and Key Characteristics of the DPANN Superphylum of Archaea
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### Summary on CRISPR in DPANN Archaea and HGT
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