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Arthrinium

Arthrinium is a genus of filamentous ascomycetous fungi belonging to the family Apiosporaceae in the order Amphisphaeriales and class Sordariomycetes.^[1] Following a 2021 taxonomic revision, it is delimited to approximately 30 accepted species worldwide (as of 2025), primarily the asexual morphs associated with Cyperaceae and Juncaceae hosts, with many former species transferred to the related genus Apiospora.^[2] These fungi are characterized by their brown, globose to ellipsoid conidia that appear lenticular in side view, featuring a distinctive equatorial slit, and are produced on cylindrical or ampulliform conidiogenous cells.^[3] The type species is A. caricicola, originally described in 1817.^[3] Species of Arthrinium exhibit a wide ecological range, functioning as endophytes, plant pathogens, or saprobes primarily on decaying plant material, soil, and various hosts including grasses, bamboos, and marine substrates such as seaweeds and sponges.^[3] They are mitosporic fungi, meaning they reproduce asexually via conidia, and have been documented in both terrestrial and marine habitats globally, with recent discoveries including eight new marine species from Korean coasts reported in 2021.^[3] While generally not pathogenic to humans, rare cases of infection have occurred, such as onychomycosis caused by Apiospora arundinis (syn. Arthrinium arundinis).^[4] Notably, certain species produce bioactive secondary metabolites, including antifungal and antioxidant compounds from marine isolates, contributing to their potential in biotechnological applications.^[3] Apiospora saccharicola (syn. Arthrinium saccharicola) is particularly significant for its production of 3-nitropropionic acid, a potent mitochondrial toxin that has caused fatal poisoning in humans through contaminated coconut water, leading to rapid encephalopathy and brain damage.^[5] The genus's diversity continues to expand with ongoing surveys, such as those on bamboos in China, highlighting its cosmopolitan distribution and adaptability.^[6]

Taxonomy and phylogeny

History and classification

The genus Arthrinium was established in 1817 by Kunze and Schmidt, with Arthrinium caricicola designated as the type species.^[7] This description was later validated by Fries in 1832, formalizing its nomenclatural status within fungal taxonomy.^[8] Initially recognized for its conidial morphology, the genus has since been subject to numerous synonymies and reclassifications as mycological understanding evolved.^[9] Key taxonomic revisions occurred in the late 20th and early 21st centuries, driven by molecular phylogenetic data. In 2013, a comprehensive re-evaluation using multi-gene analyses placed Arthrinium within the family Apiosporaceae in the order Xylariales, under the class Sordariomycetes and phylum Ascomycota.^[10] This transfer resolved earlier uncertainties about its affinities, distinguishing it from superficially similar genera in other orders.^[3] Subsequent studies have reinforced this classification through expanded datasets, including ITS and LSU rDNA sequences.^[11] The genus Arthrinium, typified by its anamorphic (asexual) state, has been traditionally connected to the teleomorphic (sexual) genus Apiospora Saccardo, established in 1882.^[12] These anamorph-teleomorph links were confirmed via morphological comparisons and molecular evidence, particularly in the 1990s and 2000s, leading to the recognition of Apiospora as the sexual morph of Arthrinium.^[10] This dual nomenclature reflects the historical separation of asexual and sexual fungal forms, now unified under the "one fungus-one name" principle in modern mycology.^[13] As of 2021, Arthrinium is accepted as comprising approximately 88 species worldwide, according to Index Fungorum.^[14] Subsequent research has expanded this diversity, with numerous species transferred to Apiospora and new taxa described, resulting in approximately 196 epithets under Apiospora (the preferred name in recent studies) as of October 2024.^[15] This tally includes both established taxa and newly described species from diverse substrates, with ongoing molecular surveys contributing to further refinements.^[7]

Phylogenetic relationships

Phylogenetic analyses of Arthrinium have primarily relied on multi-locus sequencing of nuclear ribosomal DNA regions including the internal transcribed spacer (ITS), large subunit (LSU), and small subunit (SSU), as well as protein-coding genes such as translation elongation factor 1-alpha (TEF) and the second largest subunit of RNA polymerase II (RPB2). These markers provide resolution at both generic and species levels, with ITS commonly used for species delimitation due to its variability, while LSU and SSU offer broader familial placement, and TEF and RPB2 enhance phylogenetic support in combined datasets. For instance, maximum likelihood and Bayesian inference methods applied to concatenated alignments of these loci have consistently resolved Arthrinium strains into well-supported clades, distinguishing it from closely related taxa.^[10]^[16] Arthrinium is positioned within the family Apiosporaceae (Xylariales, Sordariomycetes), forming a monophyletic group supported by high bootstrap values and posterior probabilities in multi-gene phylogenies. Within Apiosporaceae, Arthrinium appears as a distinct lineage sister to genera such as Apiospora—often regarded as its sexual morph counterpart—and Dinemasporium, based on shared synapomorphies in conidial morphology and molecular signatures. This placement has been refined through studies epitypifying the type species A. caricicola and analyzing type material, confirming the family's circumscription exclusive of unrelated coelomycetes previously misclassified under Arthrinium.^[2]^[17] Multi-locus studies have revealed distinct marine and terrestrial clades within Arthrinium, reflecting ecological adaptations and host specificities. Terrestrial strains, often from bamboos and grasses, cluster separately from marine isolates collected from coastal substrates like driftwood and algae, with genetic divergence highlighted by variations in ITS and TEF sequences. For example, analyses of combined ITS, TUB2, TEF, cmdA, and RPB2 loci from bamboo-associated taxa demonstrated robust separation of eleven clades, underscoring habitat-driven evolution. Similarly, marine-focused phylogenies using ITS, TUB, and TEF have identified habitat-specific lineages, including those from Korean intertidal zones.^[16]^[3] In 2021, eight new Arthrinium species (A. agari, A. arctoscopi, A. fermenti, A. koreanum, A. marinum, A. pusillispermum, A. sargassi, and A. taeanense) were described from marine habitats in Korea, delineated by their phylogenetic distinctiveness in ITS- and multi-locus trees. These additions expanded the genus's diversity, with the novel taxa forming independent clades sister to known marine species like A. phaeospermum, supported by bootstrap values exceeding 90%. This study emphasized the role of molecular data in uncovering cryptic diversity in underrepresented marine environments.^[3]

Morphology

Asexual reproduction

Asexual reproduction in Arthrinium primarily occurs through the production of conidia via basauxic conidiogenesis, a holoblastic process where conidiogenous cells develop from mother cells and produce conidia sympodially or through percurrent proliferation in some species.^[9] This mode is diagnostic for the genus, distinguishing it from related fungi by the basauxic conidiogenesis, characterized by proliferation of conidiogenous cells through both basal and apical growth.^[18] Conidiophores are typically simple or reduced to conidiogenous cells, arising solitarily from hyphae or aggregated in clusters on pale brown stroma that may form black sporodochia; they are cylindrical to ampulliform, hyaline to pale brown, and measure 10–150 μm in length, bearing conidia terminally, laterally, or intercalarily.^[9]^[7] Conidia of Arthrinium are aseptate, unicellular, and range from globose to ellipsoid or subglobose in surface view, often appearing lenticular in side view due to a distinctive dark equatorial germ slit; they are hyaline to dark brown, smooth to finely roughened or verruculose, and typically measure 5–15 μm in diameter, though sizes vary by species (e.g., 6–7 μm in A. arundinis).^[9]^[18] In some species, ramoconidia—elongated, chain-forming structures—may form, adding to conidial diversity, but the primary conidia are solitary or in small clusters.^[19] These features aid in species identification, with conidial color, wall texture, and the presence of the germ slit being key morphological markers.^[7] On artificial media such as potato dextrose agar (PDA), Arthrinium colonies grow effuse and fast-spreading, reaching 2–5 cm in diameter within 5–7 days at 25°C, with surfaces ranging from flat to woolly and covered in aerial mycelium.^[18] Colony colors are characteristically dark olivaceous to black or iron-grey on the surface, with reverse sides pale yellow to dark brown, often producing diffuse pigments; sporulation typically occurs after 7–10 days, enhancing the dark appearance.^[9]^[7] These cultural traits reflect the genus's saprobic nature and facilitate laboratory identification.^[19]

Sexual reproduction

The sexual reproduction of Arthrinium (asexual morph) corresponds to its teleomorphic stage in the genus Apiospora.^[9]^[15] Ascomata are typically immersed or erumpent, globose to pyriform, dark brown to black, and measure 100–300 μm in diameter, often developing beneath the host epidermis with a papillate ostiole for spore release.^[20]^[9] These structures feature walls composed of 6–9 layers of pseudoparenchymatous cells, and in some cases, they form in rows or clusters within stromata on natural substrates.^[9] Asci within the ascomata are unitunicate, cylindrical to clavate, 8-spored, and equipped with an apical pore and a short basal pedicel, typically measuring 60–110 × 10–25 μm.^[20]^[9] Ascospores are arranged bi- to tri-seriate inside the asci, fusiform to clavate with a larger upper cell and smaller lower cell, hyaline, smooth-walled, 1-septate, measuring 20–35 × 6–10 μm, with rounded ends.^[20]^[9] Some ascospores may possess a mucoid sheath, though this varies by species.^[9] The sexual stage of Arthrinium is rarely observed in culture, with most documented instances derived from field collections on natural substrates such as decaying bamboo and other plant debris.^[9]^[20] This contrasts with the more frequently encountered asexual conidial production, highlighting the challenges in inducing teleomorph formation under laboratory conditions.^[9]

Habitat and ecology

Distribution and substrates

Arthrinium exhibits a cosmopolitan distribution, occurring across temperate, tropical, subtropical, Mediterranean, and cold regions worldwide.^[21] The genus is reported in diverse geographic areas, including North and South America, Europe, Africa, Asia, and Oceania.^[22] In Asia, it is particularly prevalent in subtropical regions such as China and Korea, where strains have been isolated from bamboo leaves, tea plants, soil, and air in karst caves.^[23] In Europe, Arthrinium species have been collected from Mediterranean and temperate locations, often associated with graminaceous plants.^[24] Marine environments also host the fungus, with isolations from seaweed, sponges, and egg masses of the sailfin sandfish (Arctoscopus japonicus) along coastal sites.^[7] For instance, a 2021 study isolated 41 strains representing 14 species from eight coastal sites on the west coast of Korea and Jeju Island, highlighting its abundance in subtropical marine habitats.^[3] Arthrinium primarily colonizes graminaceous plants, including grasses (Poaceae) and sedges (Cyperaceae), as well as bamboo, plant debris, and soil.^[25] It has also been detected in indoor environments on cellulose-containing materials and in airborne samples.^[26] It has also been reported from lichens and insect guts.^[16] The fungus demonstrates adaptations to varied niches, functioning as an endophyte within living plant tissues or as a saprobe on decaying organic matter.^[3]

Ecological roles

Arthrinium species frequently adopt an endophytic lifestyle, colonizing healthy plant tissues asymptomatically and providing potential benefits to their hosts through secondary metabolite production. In terrestrial environments, they are commonly found as endophytes in grasses and reeds, such as Phragmites australis and members of the Restionaceae family, where they inhabit culms and leaves without causing visible damage. Similarly, numerous species, including A. bambusicola and A. phyllostachium, occur as endophytes in bamboo (Schizostachyum brachycladum and Phyllostachys heteroclada), contributing to plant resilience in Asian ecosystems.^[9]^[6] As saprobes, Arthrinium fungi play a vital role in decomposition processes, particularly breaking down lignocellulosic plant debris in terrestrial habitats. They colonize dead bamboo culms and grass stems, forming stromata and black spots that facilitate the degradation of complex organic matter, thereby aiding nutrient cycling by releasing essential elements back into the soil. This saprobic activity is evident in species like A. biseriale, A. guizhouense, and A. arundinis, which thrive on decaying substrates in diverse regions including China and Europe.^[6]^[9] In marine ecosystems, Arthrinium exhibits adaptations as endophytes in algae and associations with marine animals, enhancing host tolerance to environmental stresses. Species such as A. sargassi form symbiotic relationships with brown algae like Sargassum fulvellum, producing antifungal and antioxidant metabolites that combat oxidative stress and pathogens in saline conditions. Additionally, isolates from egg masses of the sailfin sandfish (Arctoscopus japonicus) demonstrate radical-scavenging capabilities, underscoring their role in marine symbiotic networks.^[3]^[27] Arthrinium interactions often involve antagonistic effects via secondary metabolites, positioning them as potential biocontrol agents against other fungi. For instance, A. saccharicola inhibits the pathogenic oomycete Asteromyces cruciatus on brown algae, reducing disease incidence through enzymatic and antifungal activities. These metabolites, including antioxidants, not only support host defense but also highlight Arthrinium's broader ecological influence in suppressing competitors in both terrestrial and marine settings.^[3]^[27]

Pathogenicity and significance

Plant diseases

Arthrinium species are recognized as plant pathogens capable of causing leaf spots, blights, and dieback in various crops, particularly affecting economically important plants through necrotic tissue damage and reduced yield.^[7] These fungi primarily infect members of the Poaceae family, including grasses and cereals such as barley and wheat, where they induce kernel blight and damping-off, respectively, leading to significant agricultural losses.^[28] Beyond grasses, Arthrinium has expanded to hosts like olives and sugarcane, exacerbating its threat to diverse farming systems worldwide. In bamboo, particularly moso bamboo (Phyllostachys edulis), Arthrinium arundinis causes culm rot, manifesting as rhomboid-shaped necrotic lesions that progress to tissue decay and plant weakening at higher altitudes (above 800 m).^[29] For olive trees (Olea europaea), Arthrinium marii (syn. Apiospora marii) has been identified as the pathogen responsible for canker, wilt, and dieback, first reported in Italy in 2020 and subsequently in Spain, where it causes branch necrosis and overall tree decline, posing risks to Mediterranean olive cultivation.^[30]^[31] Symptoms across these hosts commonly include chlorotic halos surrounding dark necrotic lesions, leaf wilting, and progressive dieback, often compounded by Arthrinium rasikravindrae's severe infections in multiple crops globally, which amplify disease severity through widespread tissue colonization. The host range of Arthrinium underscores its economic impact on agriculture, with primary associations to Poaceae crops like cereals that suffer yield reductions from blights, alongside emerging threats to olives and sugarcane, where post-harvest molds and cankers disrupt production and storage.^[7]^[32] For instance, Arthrinium arundinis (syn. Apiospora arundinis) causes mold on sugarcane in China, leading to surface discoloration and quality degradation during improper storage. Disease management remains limited, relying on preventive cultural practices such as improved sanitation and resistant varieties, supplemented by fungicide applications, though efficacy varies due to the fungi's adaptability. Advances include the first whole-genome sequence of A. rasikravindrae in 2022, which revealed genetic insights into virulence factors and supports the development of targeted control strategies.^[33]

Human and animal health effects

Arthrinium species, particularly A. saccharicola, A. phaeospermum, and A. sacchari, produce the mycotoxin 3-nitropropionic acid (3-NPA), a potent inhibitor of mitochondrial succinate dehydrogenase that can lead to severe neurotoxicity in humans upon ingestion of contaminated food sources such as moldy sugarcane or spoiled coconut water.^[34]^[35] Symptoms of 3-NPA poisoning typically begin with gastrointestinal distress including vomiting and nausea, progressing to neurological manifestations such as dystonia, encephalopathy, coma, and potentially death if untreated.^[5] Notable outbreaks have occurred in China, where ingestion of moldy sugarcane contaminated by Arthrinium spp. resulted in 884 reported cases and 88 fatalities between 1972 and 1989. A fatal case in Denmark involved a 69-year-old man who consumed coconut water spoiled by A. saccharicola, highlighting the toxin's lethality even in non-endemic regions.^[5] Human infections by Arthrinium are rare but can manifest as superficial or deep mycoses, often in immunocompromised individuals where the fungus acts as an opportunistic pathogen.^[36] Onychomycosis, or nail infections, have been documented, such as a 2020 case involving A. arundinis in a 56-year-old woman with relapsing lepromatous leprosy, presenting as subungual hyperkeratosis and discoloration treated successfully with itraconazole and amorolfine.^[37] Deeper infections are even less common; a 2024 report described the first case of carpal tunnel syndrome caused by A. phaeospermum in a male patient with hand numbness and pain, resolved through surgical debridement and 10 months of antifungal therapy.^[36] The airborne conidia of Arthrinium, commonly found in indoor environments, contribute to its allergenic potential, potentially causing respiratory irritation and exacerbating asthma in sensitized individuals, as observed in assessments of moldy buildings.^[38] Exposure to such fungal spores is associated with allergic reactions, including airway hyperresponsiveness, particularly in damp indoor settings where Arthrinium growth is favored.^[26] In animals, 3-NPA from Arthrinium-contaminated feed poses similar risks, leading to neurologic disorders in grazing livestock that ingest toxin-laden forages like certain Astragalus species.^[39] Ruminants are particularly susceptible, with the mycotoxin disrupting rumen fermentation and causing acute toxicity, though effects can be mitigated by processing feed into hay.^[40]

Species diversity

Overview of species

The genus Arthrinium encompasses over 90 accepted species worldwide, as documented in fungal databases as of 2024, reflecting ongoing taxonomic revisions including transfers to related genera like Apiospora and Neoarthrinium, and new discoveries.^[41] This count includes eight new marine species reported from coastal habitats in Korea in 2021.^[3] Species delimitation within Arthrinium relies on multi-locus phylogenetic analyses, primarily using the internal transcribed spacer (ITS) region alongside other loci such as the large subunit (LSU) rDNA, translation elongation factor 1-alpha (tef1), and beta-tubulin (tub2), combined with morphological traits like conidial shape and size.^[2] Substrate specificity also plays a key role, as species often show host or habitat preferences that support phylogenetic clustering.^[3] The distribution of Arthrinium species is predominantly terrestrial, with the majority associated with plants such as bamboos and grasses, while a smaller proportion inhabits marine environments.^[18] The genus exhibits a cosmopolitan range, though diversity hotspots occur in Asia, particularly in regions like China and Korea.^[11] The type species, A. caricicola, was originally described from stems of Carex (Cyperaceae) sedges.^[42] Recent taxonomic studies have further refined the genus, with the establishment of Neoarthrinium in 2022 accommodating four species previously in Arthrinium, and additional new species described from bamboos and other substrates in China as of 2024.^[43]^[44]

Notable species

Apiospora sphaerosperma (syn. Arthrinium phaeospermum) is a notable species within the genus due to its production of the mycotoxin 3-nitropropionic acid (3-NPA), which has been implicated in human poisonings, particularly from consumption of moldy sugarcane.^[45] This fungus is also recognized as an indoor mold contaminant, contributing to air quality issues in damp environments and occasionally causing superficial infections in humans.^[46] Its whole-genome sequence was completed in 2019, providing insights into its pathogenic mechanisms and marking the first such assembly for the genus Arthrinium.^[47] Apiospora saccharicola (syn. Arthrinium saccharicola) stands out for its role in food poisoning outbreaks, notably producing high levels of 3-NPA that contaminated coconut water and sugarcane products, leading to fatal cases with neurological symptoms.^[5]^[48] This species has been isolated from spoiled agricultural substrates, highlighting its significance in post-harvest pathology and public health risks associated with mycotoxin accumulation.^[45] Apiospora marii (syn. Arthrinium marii) emerged as a plant pathogen in 2020, identified as the causal agent of dieback in olive trees (Olea europaea) in southern Italy, where it induces bark cankers and wood discoloration.^[30] Pathogenicity tests confirmed its ability to cause complete dieback in inoculated two-year-old olive plants within six months, posing a potential threat to olive cultivation in Mediterranean regions.^[49] Apiospora arundinis (syn. Arthrinium arundinis) is significant for its association with human onychomycosis, a nail infection reported in case studies involving immunocompromised patients, such as those with leprosy, where it was isolated from affected toenails.^[37]^[4] This species is also frequently recovered from plant debris and substrates like bamboo and soil, underscoring its saprobic lifestyle alongside opportunistic pathogenicity.^[29]^[6] Among marine species, Arthrinium agari and A. arctoscopi, both described as new in 2021, exemplify the genus's adaptation to aquatic environments as endophytes. A. agari was isolated from the brown alga Agarum cribrosum (seaweed), while A. arctoscopi originated from fish eggs in Korean coastal waters, contributing to the understanding of fungal diversity in marine ecosystems with potential for bioactive metabolites, including antifungal compounds observed in related Arthrinium species.^[7]

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