Meta-omics highlights the diversity, activity and adaptations of fungi in deep oceanic crust.
Journal
Environmental microbiology
ISSN: 1462-2920
Titre abrégé: Environ Microbiol
Pays: England
ID NLM: 100883692
Informations de publication
Date de publication:
09 2020
09 2020
Historique:
received:
12
05
2020
revised:
23
07
2020
accepted:
31
07
2020
pubmed:
4
8
2020
medline:
7
4
2021
entrez:
4
8
2020
Statut:
ppublish
Résumé
The lithified oceanic crust, lower crust gabbros in particular, has remained largely unexplored by microbiologists. Recently, evidence for heterogeneously distributed viable and transcriptionally active autotrophic and heterotrophic microbial populations within low-biomass communities was found down to 750 m below the seafloor at the Atlantis Bank Gabbro Massif, Indian Ocean. Here, we report on the diversity, activity and adaptations of fungal communities in the deep oceanic crust from ~10 to 780 mbsf by combining metabarcoding analyses with mid/high-throughput culturing approaches. Metabarcoding along with culturing indicate a low diversity of viable fungi, mostly affiliated to ubiquitous (terrestrial and aquatic environments) taxa. Ecophysiological analyses coupled with metatranscriptomics point to viable and transcriptionally active fungal populations engaged in cell division, translation, protein modifications and other vital cellular processes. Transcript data suggest possible adaptations for surviving in the nutrient-poor, lithified deep biosphere that include the recycling of organic matter. These active communities appear strongly influenced by the presence of cracks and veins in the rocks where fluids and resulting rock alteration create micro-niches.
Identifiants
pubmed: 32743889
doi: 10.1111/1462-2920.15181
doi:
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Research Support, U.S. Gov't, Non-P.H.S.
Langues
eng
Sous-ensembles de citation
IM
Pagination
3950-3967Subventions
Organisme : Deutsche Forschungsgemeinschaft
ID : EXC-2077-390741603
Pays : International
Organisme : National Science Foundation of China
ID : 31872615
Pays : International
Organisme : National Science Foundation
ID : OCE-1658118
Pays : International
Organisme : National Science Foundation
ID : OCE-1658031
Pays : International
Informations de copyright
© 2020 Society for Applied Microbiology and John Wiley & Sons Ltd.
Références
Amend, A. (2014) From dandruff to deep-sea vents: Malassezia-like fungi are ecologically hyper-diverse. PLoS Pathog 10: e1004277.
Baehrecke, E.H. (2005) Autophagy: dual roles in life and death? Nat Rev Mol Cell Biol 6: 505-510.
Bass, D., Howe A., Brown N., Barton, H., Demidova, M., Michelle, H., et al. (2007) Yeast forms dominate fungal diversity in the deep oceans. Proc Roy Soc B Biol Sci 274(1629): 3069-3077. http://dx.doi.org/10.1098/rspb.2007.1067.
Bengtson, S., Ivarsson, M., Astolfo, A., Belivanova, V., Broman, C., Marone, F., and Stampanoni, M. (2014) Deep-biosphere consortium of fungi and prokaryotes in Eocene subseafloor basalts. Geobiology 12: 489-496.
Bengtson, S., Rasmussen, B., Ivarsson, M., Muhling, J., Broman, C., Marone, F., et al. (2017) Fungus-like mycelial fossils in 2.4-billion-year-old vesicular basalt. Nat Ecol Evol 1: 0141.
Bengtsson-Palme, J., Ryberg, M., Hartmann, M., Branco, S., Wang, Z., Godhe, A., et al. (2013) Improved software detection and extraction of ITS1 and ITS2 from ribosomal ITS sequences of fungi and other eukaryotes for analysis of environmental sequencing data. Methods Ecol Evol 4: 914-919.
Boratyn, G.M., Thierry-Mieg, J., Thierry-Mieg, D., Busby, B., and Madden, T.L. (2019) Magic-BLAST, an accurate RNA-seq aligner for long and short reads. BMC Bioinformatics 20: 405.
Bradley, J.A., Amend, J.P., and LaRowe, D.E. (2018) Necromass as a limited source of energy for microorganisms in marine sediments. J Geophys Res Biogeosci 123: 577-590.
Braun, S., Mhatre, S.S., Jaussi, M., Røy, H., Kjeldsen, K.U., Pearce, C., et al. (2017) Microbial turnover times in the deep seabed studied by amino acid racemization modelling. Sci Rep 7: 1-14.
Burgaud, G., Arzur, D., Durand, L., Cambon-Bonavita, M.-A., and Barbier, G. (2010) Marine culturable yeasts in deep-sea hydrothermal vents: species richness and association with fauna: culturable yeasts from hydrothermal vents. FEMS Microbiol Ecol 73: 121-133.
Burgaud, G., Calvez, T., Arzur, D., Vandenkoornhuyse, P., and Barbier, G. (2009) Diversity of culturable marine filamentous fungi from deep-sea hydrothermal vents. Environ Microbiol 11: 1588-1600.
Burgaud, G., Hué, N., Arzur, D., Coton, M., Perrier-Cornet, J.-M., Jebbar, M., and Barbier, G. (2015) Effects of hydrostatic pressure on yeasts isolated from deep-sea hydrothermal vents. Res Microbiol 166: 700-709.
Callahan, B.J., McMurdie, P.J., Rosen, M.J., Han, A.W., Johnson, A.J.A., and Holmes, S.P. (2016) DADA2: high resolution sample inference from Illumina amplicon data. Nat Methods 13: 581-583.
Calvez, T.L. (2009) Diversité et fonctions écologiques des champignons en écosystème hydrothermal marin profond.
Ciobanu, M.-C., Burgaud, G., Dufresne, A., Breuker, A., Rédou, V., Ben Maamar, S., et al. (2014) Microorganisms persist at record depths in the subseafloor of the Canterbury Basin. ISME J 8: 1370-1380.
Cobo-Díaz, J.F., Baroncelli R., Le Floch, G., and Picot, A. (2019) A novel metabarcoding approach to investigate Fusarium species composition in soil and plant samples. FEMS Microbiol Ecol 95(7). http://dx.doi.org/10.1093/femsec/fiz084
Cunliffe, M., Hollingsworth, A., Bain, C., Sharma, V., and Taylor, J.D. (2017) Algal polysaccharide utilisation by saprotrophic planktonic marine fungi. Fungal Ecol 30: 135-138.
D'Hondt, S., Spivack, A.J., Pockalny, R., Ferdelman, T.G., Fischer, J.P., Kallmeyer, J., et al. (2009) Subseafloor sedimentary life in the South Pacific Gyre. Proc Natl Acad Sci U S A 106: 11651-11656.
Damare, S., Raghukumar, C., and Raghukumar, S. (2006) Fungi in deep-sea sediments of the Central Indian Basin. Deep-Sea Res I Oceanogr Res Pap 53: 14-27.
Dekov, V., Bindi, L., Burgaud, G., Petersen, S., Asael, D., Rédou Creff, V., et al. (2013) Inorganic and biogenic As-sulfide precipitation at seafloor hydrothermal fiels. Mar Geol 342: 28-38.
Dover, C.E., Ward, M.L., Scott, J., Underdown, J., Anderson, B., Gustafson, C., et al. (2007) A fungal epizootic in mussels at a deep-sea hydrothermal vent. Mar Ecol 28: 54-62.
Drake, H., and Ivarsson, M. (2017) The role of anaerobic fungi in fundamental biogeochemical cycles in the deep biosphere. Fungal Biol Rev 32: 20-25.
Drake, H., Ivarsson, M., Bengtson, S., Heim, C., Siljeström, S., Whitehouse, M.J., et al. (2017) Anaerobic consortia of fungi and sulfate reducing bacteria in deep granite fractures. Nat Commun 8: 55.
Edgcomb, V.P., Beaudoin, D., Gast, R., Biddle, J.F., and Teske, A. (2011) Marine subsurface eukaryotes: the fungal majority. Environ Microbiol 13: 172-183.
Edgcomb, V.P., Pachiadaki, M.G., Mara, P., Kormas, K.A., Leadbetter, E.R., and Bernhard, J.M. (2016) Gene expression profiling of microbial activities and interactions in sediments under haloclines of E. Mediterranean deep hypersaline anoxic basins. ISME J 10: 2643-2657.
Ekendahl, S., O'Neill, A.H., Thomsson, E., and Pedersen, K. (2003) Characterisation of yeasts isolated from deep igneous rock aquifers of the Fennoscandian Shield. Microb Ecol 46: 416-428.
Embley, T.M., van der Giezen, M., Horner, D.S., Dyal, P.L., Bell, S., and Foster, P.G. (2003) Hydrogenosomes, mitochondria and early eukaryotic evolution. IUBMB Life 55: 387-395.
Emri, T., Molnár, Z., and Pócsi, I. (2005) The appearances of autolytic and apoptotic markers are concomitant but differently regulated in carbon-starving Aspergillus nidulans cultures. FEMS Microbiol Lett 251: 297-303.
Engelen, B., Ziegelmüller, K., Wolf, L., Köpke, B., Gittel, A., Cypionka, H., et al. (2008) Fluids from the oceanic crust support microbial activities within the deep biosphere. Geomicrobiol J 25: 56-66.
Gaboyer, F., Burgaud, G., and Edgcomb, V. (2019) The deep subseafloor and biosignatures. In Biosignatures for Astrobiology, Cavalazzi, B., and Westall, F. (eds). Cham: Springer International Publishing, pp. 87-109.
García-Lepe, R., Nuero, O.M., Reyes, F., and Santamaría, F. (1997) Lipases in autolysed cultures of filamentous fungi. Lett Appl Microbiol 25: 127-130.
Gladfelter, A.S., James, T.Y., and Amend, A.S. (2019) Marine fungi. Curr Biol 29: R191-R195.
Hackstein, J.H.P., Baker, S.E., van Hellemond, J.J., and Tielens, A.G.M. (2019) Hydrogenosomes of anaerobic fungi: an alternative way to adapt to anaerobic environments. In Hydrogenosomes and Mitosomes: Mitochondria of Anaerobic Eukaryotes. Microbiology Monographs, Tachezy, J. (ed). Cham: Springer International Publishing, pp. 159-175.
Hassett, B.T., Ducluzeau, A.-L.L., Collins, R.E., and Gradinger, R. (2017) Spatial distribution of aquatic marine fungi across the western Arctic and sub-arctic. Environ Microbiol 19: 475-484.
Hassett, B.T., and Gradinger, R. (2018) New species of Saprobic Labyrinthulea (=Labyrinthulomycota) and the erection of a gen. nov. to resolve molecular polyphyly within the Aplanochytrids. J Eukaryotic Microbiol 65: 475-483.
Hirayama, H., Nagano, Y., Abe, M., Miyazaki, J., Sakai, S., and Takai, K. (2015) Data report: cultivation of microorganisms from basaltic rock and sediment cores from the north pond on the western flank of the mid-Atlantic ridge, IODP expedition. Proc Integr Ocean Drill Program 336: 12.
Hynes, M.J., Murray, S.L., Duncan, A., Khew, G.S., and Davis, M.A. (2006) Regulatory genes controlling fatty acid catabolism and peroxisomal functions in the filamentous fungus Aspergillus nidulans. Eukaryot Cell 5: 794-805.
Hynes, M.J., Murray, S.L., Khew, G.S., and Davis, M.A. (2008) Genetic analysis of the role of peroxisomes in the utilization of acetate and fatty acids in Aspergillus nidulans. Genetics 178: 1355-1369.
Inagaki, F., Hinrichs, K.-U., Kubo, Y., Bowles, M.W., Heuer, V.B., Hong, W.-L., et al. (2015) Deep Biosphere. Exploring deep microbial life in coal-bearing sediment down to ~2.5 km below the ocean floor. Science 349: 420-424.
Ivarsson, M., Bengtson, S., Belivanova, V., Stampanoni, M., Marone, F., and Tehler, A. (2011a) Fossilized fungi in subseafloor Eocene basalts. Geology 40: 163-166.
Ivarsson, M., Bengtson, S., and Neubeck, A. (2016a) The igneous oceanic crust - Earth's largest fungal habitat? Fungal Ecol 20: 249-255.
Ivarsson, M., Bengtson, S., Skogby, H., Lazor, P., Broman, C., Belivanova, V., and Marone, F. (2015a) A fungal-prokaryotic consortium at the basalt-zeolite interface in subseafloor igneous crust. PLoS One 10: e0140106.
Ivarsson, M., Broman, C., Gustafsson, H., and Holm, N.G. (2015b) Biogenic Mn-oxides in subseafloor basalts. PLoS One 10: e0128863.
Ivarsson, M., Broman, C., and Holm, N.G. (2011b) Chromite oxidation by manganese oxides in subseafloor basalts and the presence of putative fossilized microorganisms. Geochem Trans 12: 5.
Ivarsson, M., Broman, C., Holmström, S.J.M., Ahlbom, M., Lindblom, S., and Holm, N.G. (2011c) Putative fossilized fungi from the lithified volcaniclastic apron of Gran Canaria, Spain. Astrobiology 11: 633-650.
Ivarsson, M., Peckmann, J., Tehler, A., Broman, C., Bach, W., Behrens, K., et al. (2015c) Zygomycetes in vesicular basanites from Vesteris Seamount, Greenland Basin - a new type of Cryptoendolithic fungi. PLoS One 10: e0133368.
Ivarsson, M., Schnürer, A., Bengtson, S., and Neubeck, A. (2016b) Anaerobic fungi: a potential source of biological H2 in the oceanic crust. Front Microbiol 7: 674.
Jørgensen, B.B., and Marshall, I.P.G. (2016) Slow microbial life in the seabed. Ann Rev Mar Sci 8: 311-332.
Jungbluth, S.P., Bowers, R.M., Lin, H.-T., Cowen, J.P., and Rappé, M.S. (2016) Novel microbial assemblages inhabiting crustal fluids within mid-ocean ridge flank subsurface basalt. ISME J 10: 2033-2047.
Kelley, D.S., Karson, J.A., Früh-Green, G.L., Yoerger, D.R., Shank, T.M., Butterfield, D.A., et al. (2005) A serpentinite-hosted ecosystem: the lost City hydrothermal field. Science 307: 1428-1434.
Kim, Y., Islam, N., Moss, B.J., Nandakumar, M.P., and Marten, M.R. (2011) Autophagy induced by rapamycin and carbon-starvation have distinct proteome profiles in Aspergillus nidulans. Biotechnol Bioeng 108: 2705-2715.
Li, J., Mara, P., Schubotz, F., Sylvan, J.B., Burgaud, G., Klein, F., et al. (2020) Recycling and metabolic flexibility dictate life in the lower oceanic crust. Nature 579: 250-255.
Li, W., Wang, M., Burgaud, G., Yu, H., and Cai, L. (2019) Fungal community composition and potential depth-related driving factors impacting distribution pattern and trophic modes from epi- to abyssopelagic zones of the Western Pacific Ocean. Microb Ecol 78: 820-831.
Li, W., Wang, M.M., Wang, X.G., Cheng, X.L., Guo, J.J., Bian, X.M., and Cai, L. (2016) Fungal communities in sediments of subtropical Chinese seas as estimated by DNA metabarcoding. Sci Rep 6: 26528.
Liu, C.-H., Huang, X., Xie, T.-N., Duan, N., Xue, Y.-R., Zhao, T.-X., et al. (2017) Exploration of cultivable fungal communities in deep coal-bearing sediments from ∼1.3 to 2.5 km below the ocean floor. Environ Microbiol 19: 803-818.
Liu, T.-B., and Xue, C. (2011) The ubiquitin-proteasome system and F-box proteins in pathogenic fungi. Mycobiology 39: 243-248.
Lomstein, B., Langerhuus, A., D'Hondt, S., Jørgensen, B., and Spivack, A. (2012) Endospore abundance, microbial growth and necromass turnover in deep sub-seafloor sediment. Nature 484: 101-104.
Manohar, C.S., Menezes, L.D., Ramasamy, K.P., and Meena, R.M. (2014) Phylogenetic analyses and nitrate-reducing activity of fungal cultures isolated from the permanent, oceanic oxygen minimum zone of the Arabian Sea. Can J Microbiol 61: 217-226.
Meyer, J.L., Jaekel, U., Tully, B.J., Glazer, B.T., Wheat, C.G., Lin, H.-T., et al. (2016) A distinct and active bacterial community in cold oxygenated fluids circulating beneath the western flank of the mid-Atlantic ridge. Sci Rep 6: 22541.
Nagano, Y., Miura, T., Nishi, S., Lima, A.O., Nakayama, C., Pellizari, V.H., and Fujikura, K. (2017) Fungal diversity in deep-sea sediments associated with asphalt seeps at the Sao Paulo Plateau. Deep-Sea Res II Top Stud Oceanogr 146: 59-67.
Nagano, Y., Nagahama, T., Hatada, Y., Nunoura, T., Takami, H., Miyazaki, J., et al. (2010) Fungal diversity in deep-sea sediments - the presence of novel fungal groups. Fungal Ecol 3: 316-325.
Navarri, M., Jégou, C., Meslet-Cladière, L., Brillet, B., Barbier, G., Burgaud, G., and Fleury, Y. (2016) Deep subseafloor fungi as an untapped reservoir of amphipathic antimicrobial compounds. Mar Drugs 14: 50.
Nilsson, R.H., Larsson, K.-H., Taylor, A.F.S., Bengtsson-Palme, J., Jeppesen, T.S., Schigel, D., et al. (2019) The UNITE database for molecular identification of fungi: handling dark taxa and parallel taxonomic classifications. Nucleic Acids Res 47: D259-D264.
Oger, P.M., and Jebbar, M. (2010) The many ways of coping with pressure. Res Microbiol 161: 799-809.
Orcutt, B.N., LaRowe, D.E., Biddle, J.F., Colwell, F.S., Glazer, B.T., Reese, B.K., et al. (2013) Microbial activity in the marine deep biosphere: progress and prospects. Front Microbiol 4: 189.
Orcutt, B.N., Bach, W., Becker, K., Fisher, A.T., Hentscher, M., Toner, B.M., et al. (2011a) Colonization of subsurface microbial observatories deployed in young ocean crust. ISME J 5: 692-703.
Orcutt, B.N., Sylvan, J.B., Knab, N.J., and Edwards, K.J. (2011b) Microbial ecology of the Dark Ocean above, at, and below the seafloor. Microbiol Mol Biol Rev 75: 361-422.
Orsi, W., Biddle, J.F., and Edgcomb, V. (2013) Deep sequencing of subseafloor eukaryotic rRNA reveals active fungi across marine subsurface provinces. PLoS One 8: e56335.
Orsi, W.D. (2018) Ecology and evolution of seafloor and subseafloor microbial communities. Nat Rev Microbiol 16: 671-683.
Orsi, W.D., Richards, T.A., and Francis, W.R. (2018) Predicted microbial secretomes and their target substrates in marine sediment. Nat Microbiol 3(1): 32-37. http://dx.doi.org/10.1038/s41564-017-0047-9
Pachiadaki, M.G., Rédou, V., Beaudoin, D.J., Burgaud, G., and Edgcomb, V.P. (2016) Fungal and prokaryotic activities in the marine subsurface biosphere at Peru margin and Canterbury Basin inferred from RNA-based analyses and microscopy. Front Microbiol 7: 846.
Pang, K.-L., Guo, S.-Y., Chen, I.-A., Burgaud, G., Luo, Z.-H., Dahms, H.U., et al. (2019) Insights into fungal diversity of a shallow-water hydrothermal vent field at Kueishan Island, Taiwan by culture-based and metabarcoding analyses. PLoS One 14: e0226616.
Parkes, R., Cragg, B., Roussel, E.G., Webster, G., Weightman, A., and Sass, H. (2014) A review of prokaryotic populations and processes in sub-seafloor sediments, including biosphere:geosphere interactions. Mar Geol 352: 409-425.
Polinski, J.M., Bucci, J.P., Gasser, M., and Bodnar, A.G. (2019) Metabarcoding assessment of prokaryotic and eukaryotic taxa in sediments from Stellwagen Bank National Marine Sanctuary. Sci Rep 9: 1-8.
Raghukumar, C., Damare, S., and Singh, P. (2010) A review on deep-sea fungi: occurrence, diversity and adaptations. Bot Mar 53: 479-492.
Raghukumar, S. (2006) Marine microbial eukaryotic diversity, with particular reference to fungi: lessons from prokaryotes. Indian J Mar Sci 35: 11.
Rédou, V., Ciobanu, M.C., Pachiadaki, M.G., Edgcomb, V., Alain, K., Barbier, G., and Burgaud, G. (2014) In-depth analyses of deep subsurface sediments using 454-pyrosequencing reveals a reservoir of buried fungal communities at record-breaking depths. FEMS Microbiol Ecol 90: 908-921.
Rédou, V., Navarri, M., Meslet-Cladière, L., Barbier, G., and Burgaud, G. (2015) Species richness and adaptation of marine fungi from deep-subseafloor sediments. Appl Environ Microbiol 81: 3571-3583.
Santelli, C.M., Edgcomb, V.P., Bach, W., and Edwards, K.J. (2009) The diversity and abundance of bacteria inhabiting seafloor lavas positively correlate with rock alteration. Environ Microbiol 11: 86-98.
Schrenk, M.O., Brazelton, W.J., and Lang, S.Q. (2013) Serpentinization, carbon, and deep life. Rev Mineral Geochem 75: 575-606.
Sheridan, K.J., Dolan, S.K., and Doyle, S. (2015) Endogenous cross-talk of fungal metabolites. Front Microbiol 5: 732.
Staszczak, M. (2008) The role of the ubiquitin-proteasome system in the response of the ligninolytic fungus Trametes versicolor to nitrogen deprivation. Fungal Genet Biol 45: 328-337.
Szilágyi, M., Miskei, M., Karányi, Z., Lenkey, B., Pócsi, I., and Emri, T. (2013) Transcriptome changes initiated by carbon starvation in aspergillus nidulans. Microbiology (Reading, Engl) 159: 176-190.
Tedersoo, L., Anslan, S., Bahram, M., Põlme, S., Riit, T., Liiv, I., et al. (2015) Shotgun metagenomes and multiple primer pair-barcode combinations of amplicons reveal biases in metabarcoding analyses of fungi. MycoKeys 10: 1-43.
Thomas, C., Grossi, V., Antheaume, I., and Ariztegui, D. (2019) Recycling of archaeal biomass as a new strategy for extreme life in Dead Sea deep sediments. Geology 47: 479-482.
Tielens, A.G.M., Rotte, C., van Hellemond, J.J., and Martin, W. (2002) Mitochondria as we don't know them. Trends Biochem Sci 27: 564-572.
van der Giezen, M., Birdsey, G.M., Horner, D.S., Lucocq, J., Dyal, P.L., Benchimol, M., et al. (2003) Fungal hydrogenosomes contain mitochondrial heat-shock proteins. Mol Biol Evol 20: 1051-1061.
Xu, W., Gong, L., Pang, K.-L., and Luo, Z.-H. (2018) Fungal diversity in deep-sea sediments of a hydrothermal vent system in the Southwest Indian Ridge. Deep-Sea Res I Oceanogr Res Pap 131: 16-26.
Yanagawa, K., Breuker, A., Schippers, A., Nishizawa, M., Ijiri, A., Hirai, M., et al. (2014) Microbial community stratification controlled by the subseafloor fluid flow and geothermal gradient at the Iheya north hydrothermal field in the mid-Okinawa trough (Integrated Ocean Drilling Program Expedition 331). Appl Environ Microbiol 80: 6126-6135.
Yarlett, N., and Hackstein, J.H.P. (2005) Hydrogenosomes: One organelle, multiple origins. Bioscience 55: 657-668.
Zhang, X., Feng, X., and Wang, F. (2016) Diversity and metabolic potentials of subsurface crustal microorganisms from the Western flank of the mid-Atlantic ridge. Front Microbiol 7: 363.
Zhu, R., Versteegh, G.J.M., and Hinrichs, K.-U. (2016) Detection of microbial biomass in subseafloor sediment by pyrolysis-GC/MS. J Anal Appl Pyrolysis 118: 175-180.
Zinke, L.A., Glombitza, C., Bird, J.T., Røy, H., Jørgensen, B.B., Lloyd, K.G., et al. (2019) Microbial organic matter degradation potential in Baltic Sea sediments is influenced by depositional conditions and in situ geochemistry. Appl Environ Microbiol 85(4).