Carbon assimilating fungi from surface ocean to subseafloor revealed by coupled phylogenetic and stable isotope analysis
1.Doney S, Abbott MR, Cullen JJ, Karl DM, Rothstein L. From genes to ecosystems: the ocean’s new frontier. Ecol Environ. 2004;2:457–66.
Google Scholar
2.Field CB, Behrenfeld MJ, Randerson JT, Falkowski P. Primary production of the biosphere: integrating terrestrial and oceanic components. Science. 1998;281:237–40.CAS
PubMed
Google Scholar
3.Eppley RW, Petersen BJ. Particulate organic matter flux and planktonic new production in the deep ocean. Nature. 1979;282:677–80.
Google Scholar
4.Ducklow H, Steinberg DK, Buessler KO. Upper ocean carbon export and the biological pump. Oceanography. 2001;14:56–58.
Google Scholar
5.Carlson C, Ducklow H. Dissolved organic carbon in the upper ocean of the central equatorial Pacific Ocean, 1992: Daily and finescale vertical variations. Deep Sea Res II. 1995;42:639–56.CAS
Google Scholar
6.Cho BC, Azam F. Major role of bacteria in biogeochemical fluxes in the ocean’s interior. Nature. 1988;332:441–3.CAS
Google Scholar
7.Duarte CM, Cebrian J. The fate of marine autotrophic production. Limnol Oceanogr. 1996;41:1758–66.CAS
Google Scholar
8.Ducklow H. The bacterial component of the oceanic euphotic zone. FEMS Microbiol Ecol. 1999;30:1–30.CAS
Google Scholar
9.Herndl GJ, Reinthaler T. Microbial control of the dark end of the biological pump. Nat Geosci. 2013;6:718–24.CAS
PubMed
PubMed Central
Google Scholar
10.Worden AZ, Follows MJ, Giovannoni SJ, Wilken S, Zimmerman AE, Keeling PJ. Environmental science. Rethinking the marine carbon cycle: factoring in the multifarious lifestyles of microbes. Science. 2015;347:1257594.PubMed
Google Scholar
11.Grossart HP, Rojas-Jimenez K. Aquatic fungi: targeting the forgotten in microbial ecology. Curr Opin Microbiol. 2016;31:140–5.PubMed
Google Scholar
12.Richards TA, Jones MD, Leonard G, Bass D. Marine fungi: their ecology and molecular diversity. Ann Rev Mar Sci. 2012;4:495–522.PubMed
Google Scholar
13.Burgaud G, Arzur D, Durand L, Cambon-Bonavita MA, Barbier G. Marine culturable yeasts in deep-sea hydrothermal vents: species richness and association with fauna. FEMS Microbiol Ecol. 2010;73:121–33.CAS
PubMed
Google Scholar
14.Burgaud G, Le Calvez T, Arzur D, Vandenkoornhuyse P, Barbier G. Diversity of culturable marine filamentous fungi from deep-sea hydrothermal vents. Environ Microbiol. 2009;11:1588–1600.PubMed
Google Scholar
15.Redou V, Navarri M, Meslet-Cladiere L, Barbier G, Burgaud G. Species richness and adaptation of marine fungi from deep-subseafloor sediments. Appl Environ Microbiol. 2015;81:3571–83.CAS
PubMed
PubMed Central
Google Scholar
16.Hyde KD, Jones EBG, Leao E, Pointing SB, Poonyth AD, Vrjmoed LLP. Role of fungi in marine ecosystems. Biodivers Conserv. 1998;7:1147–61.
Google Scholar
17.Jones EB. Marine fungi: some factors influencing biodiversity. Fungal Diversity. 2000;4:53–73.
Google Scholar
18.Priest T, Fuchs B, Amann R, Reich M. Diversity and biomass dynamics of unicellular marine fungi during a spring phytoplankton bloom. Environ Microbiol. 2021;23:448–63.CAS
PubMed
Google Scholar
19.Gutierrez MH, Jara AM, Pantoja S. Fungal parasites infect marine diatoms in the upwelling ecosystem of the Humboldt current system off central Chile. Environ Microbiol. 2016;18:1646–53.PubMed
Google Scholar
20.Gutierrez MH, Pantoja S, Tejos E. The role of fungi in processing marine organic matter in the upwelling ecosystem off Chile. Mar Biol. 2011;158:205–19.
Google Scholar
21.Bochdansky AB, Clouse MA, Herdl GJ. Eukaryotic microbes, principally fungi and labyrinthulomycetes, dominate biomass on bathypelagic marine snow. ISME J. 2017;11:362–73.PubMed
Google Scholar
22.Becker S, Tebben J, Coffinet S, Wittshire K, Iversen MH, Harder T, et al. Laminarin is a major molecule in the marine carbon cycle. Proc Natl Acad Sci USA. 2020;117:6599–607.CAS
PubMed
PubMed Central
Google Scholar
23.Seymour JR, Amin SA, Raina JB, Stocker R. Zooming in on the phycosphere: the ecological interface for phytoplankton-bacteria relationships. Nat Microbiol. 2017;2:17065.CAS
PubMed
Google Scholar
24.Hassett BT, Gradinger R. Chytrids dominate arctic fungal communities. Environ Microbiol. 2016;18:2001–9.CAS
PubMed
Google Scholar
25.Lavik G, Stuhrmann T, Bruchert V, Van der Plas A, Mohrholz V, Lam P, et al. Detoxification of sulphidic African shelf waters by blooming chemolithotrophs. Nature. 2009;457:581–4.CAS
PubMed
Google Scholar
26.Ortega-Arbulu AS, Pichler M, Vuillemin A, Orsi WD. Effects of organic matter and low oxygen on the mycobenthos in a coastal lagoon. Environ Microbiol 2019;21:374–88.CAS
PubMed
Google Scholar
27.Orsi WD, Morard R, Vuillemin A, Eitel M, Wörheide G, Milucka J, et al. Anaerobic metabolism of Foraminifera thriving below the seafloor. ISME J. 2020;14:2580–94.CAS
PubMed
PubMed Central
Google Scholar
28.Orsi WD, Vuillemin A, Rodriguez P, Coskun OK, Gomez-Saez GV, Lavik G, et al. Metabolic activity analyses demonstrate that Lokiarchaeon exhibits homoacetogenesis in sulfidic marine sediments. Nat Microbiol. 2020;5:248–55.CAS
PubMed
Google Scholar
29.Dittmar T, Koch B, Hertkorn N, Kattner G. A simple and efficient method for the solid-phase extraction of dissolved organic matter (SPE-DOM) from seawater. Limnology and Oceanography. Methods. 2008;6:230–5.CAS
Google Scholar
30.Green NW, Perdue EM, Aiken GR, Butler KD, Chen H, Dittmar T, et al. An intercomparison of three methods for the large-scale isolation of oceanic dissolved organic matter. Mar Chem. 2014;161:14–19.CAS
Google Scholar
31.Riedel T, Dittmar T. A method detection limit for the analysis of natural organic matter via Fourier transform ion cyclotron resonance mass spectrometry. Anal Chem. 2014;86:8376–82.CAS
PubMed
Google Scholar
32.Merder J, Freund JA, Feudel U, Hansen CT, Hawkes JA, Jacob B, et al. ICBM-OCEAN: processing ultrahigh-resolution mass spectrometry data of complex molecular mixtures. Anal Chem. 2020;92:6832–8.CAS
PubMed
Google Scholar
33.Koch BP, Dittmar T. From mass to structure: an aromaticity index for high resolution mass data of natural organic matter. Rapid Commun Mass Spectrom. 2006;20:926–32.CAS
Google Scholar
34.Koch BP, Dittmar T. Erratum: from mass to structure: an aromaticity index for high resolution mass data of natural organic matter. Rapid Commun Mass Spectrom. 2016;20:250–250.
Google Scholar
35.Oksanen J, Blanchen FG, Friendly M, Kindt R, Legendre R, McGlinn D, et al. Vegan: community ecology package. R package version 2 4-3 2017. (https://CRAN.R-project.org/package=vegan). Accessed June 2020.36.Hansen CT, Niggemann J, Giebel HA, Simon M, Bach W, Dittmar T. Biodegradability of hydrothermally altered deep-sea dissolved organic matter. Mar Chem. 2019;217. https://doi.org/10.1016/j.marchem.2019.103706.37.Orsi WD, Smith JM, Liu S, Liu Z, Sakamoto CM, Wilken S, et al. Diverse, uncultivated bacteria and archaea underlying the cycling of dissolved protein in the ocean. ISME J. 2016;10:2158–73.CAS
PubMed
PubMed Central
Google Scholar
38.Gardes M, Bruns TD. ITS primers with enhanced specificity for basidiomycetes-application to the identification of mycorrhizae and rusts. Mol Ecol. 1993;2:113–8.CAS
PubMed
Google Scholar
39.White TJ, Bruns S, Lee S, Taylor J “Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics”. In: M Innis, D Gelfand, K Sninsky, T White, editors. PCR Protocols: a guide to methods and applications. Academic Pres, New York, NY; 1990. pp. 315–22.40.Tedersoo L, Lindahl B. Fungal identification biases in microbiome projects. Environ Microbiol Rep. 2016;8:774–9.PubMed
Google Scholar
41.Edgar RC. UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods. 2013;10:996–8.CAS
PubMed
Google Scholar
42.Nilsson RH, Larsson KH, Taylor AFS, Bengtsson-Palme J, Jeppesen TS, Schigel D, et al. The UNITE database for molecular identification of fungi: handling dark taxa and parallel taxonomic classifications. Nucleic Acids Res. 2019;47:D259–D264.CAS
PubMed
Google Scholar
43.Bolyen E, Rideout JR, Dillon MR, Bokulich NA, Abnet CC, Al-Ghalith GA, et al. Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nat Biotechnol. 2019;37:852–7.CAS
PubMed
PubMed Central
Google Scholar
44.Coskun OK, Pichler M, Vargas S, Gilder S, Orsi WD. Linking uncultivated microbial populations and benthic carbon turnover by using quantitative stable isotope probing. Appl Environ Microbiol. 2018;84:e01083–18.CAS
PubMed
PubMed Central
Google Scholar
45.Chemidlin Prevost-Boure N, Christen R, Dequiedt S, Mougel C, Lellevre M, Jolivet C, et al. Validation and application of a PCR primer set to quantify fungal communities in the soil environment by real-time quantitative PCR. PLoS One. 2011;6:e24166.CAS
PubMed
PubMed Central
Google Scholar
46.Banos S, Lentendu G, Kopf A, Wubet T, Glockner FO, Reich M. A comprehensive fungi-specific 18S rRNA gene sequence primer toolkit suited for diverse research issues and sequencing platforms. BMC Microbiol. 2018;18:190.CAS
PubMed
PubMed Central
Google Scholar
47.Haas BJ, Papanicolaou A, Yassour M, Grabherr M, Blood PD, Bowden J, et al. De novo transcript sequence reconstruction from RNA-seq using the Trinity platform for reference generation and analysis. Nat Protoc. 2013;8:1494–512.CAS
PubMed
Google Scholar
48.Buchfink B, Xie C, Huson DH. Fast and sensitive protein alignment using DIAMOND. Nat Methods. 2015;12:59–60.CAS
PubMed
Google Scholar
49.Keeling PJ, Burki F, Wilcox HM, Allam B, Allen EE, Amaral-Zettler LA, et al. The marine microbial eukaryote transcriptome sequencing project (MMETSP): illuminating the functional diversity of eukaryotic life in the oceans through transcriptome sequencing. PLoS Biol. 2014;12:e1001889.PubMed
PubMed Central
Google Scholar
50.Tatusov RL, Koonin EV, Lipman DJ. A genomic perspective on protein families. Science. 1997;278:631–7.CAS
PubMed
Google Scholar
51.Edgar RC. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 2004;32:1792–7.CAS
PubMed
PubMed Central
Google Scholar
52.Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, Gascuel O, et al. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol. 2010;59:307–21.CAS
PubMed
Google Scholar
53.Gouy M, Guindon S, Gascuel O. SeaView version 4: a multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Mol Biol Evol. 2010;27:221–4.CAS
PubMed
Google Scholar
54.Lombard V, Golaconda Ramulu H, Drula E, Coutinho PM, Henrissat B. The carbohydrate-active enzymes database (CAZy) in 2013. Nucleic Acids Res. 2014;42:D490–495.CAS
PubMed
PubMed Central
Google Scholar
55.Tamames J, Puente-Sanchez F. SqueezeMeta, a highly portable, fully automatic metagenomic analysis pipeline. Front Microbiol. 2018;9:3349.PubMed
Google Scholar
56.Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics. 2014;30:2114–20.CAS
PubMed
PubMed Central
Google Scholar
57.Li D, Liu CM, Luo R, Sadakane K, Lam TW. MEGAHIT: an ultra-fast single-node solution for large and complex metagenomics assembly via succinct de Bruijn graph. Bioinformatics. 2015;31:1674–6.CAS
PubMed
Google Scholar
58.Seemann T. Prokka: rapid prokaryotic genome annotation. Bioinformatics. 2014;30:2068–9.CAS
PubMed
Google Scholar
59.Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, et al. QIIME allows analysis of high-throughput community sequencing data. Nat Methods. 2010;7:335–6.CAS
PubMed
PubMed Central
Google Scholar
60.Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, et al. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res. 2013;41:D590–596.CAS
PubMed
Google Scholar
61.Edgar RC. MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinforma. 2004;5:1–19.
Google Scholar
62.Guillard RRL, Hargraves PE. Stichochrysis immobilis is a diatom, not a chrysophyte. Phycologia. 1993;32:234–6.
Google Scholar
63.Inthorn M, Wagner T, Scheeder G, Zabel M. Lateral transport controls distribution, quality and burial of organic matter along continental slopes in high-productivity areas. Geology. 2006;34:205–8.CAS
Google Scholar
64.Hungate BA, Mau RL, Schwartz E, Caporaso JG, Dijkstra P, van Gestel N, et al. Quantitative microbial ecology through stable isotope probing. Appl Environ Microbiol. 2015;81:7570–81.CAS
PubMed
PubMed Central
Google Scholar
65.Igarza M, Dittmar T, Graco M, Niggemann J. Dissolved organic matter cycling in the coastal upwelling system off central Peru during an “El Niño” year. Front Mar Sci. 2019;6:198.
Google Scholar
66.Kuypers MM, Lavik G, Woebken D, Schmid M, Fuchs BM, Amann R, et al. Massive nitrogen loss from the Benguela upwelling system through anaerobic ammonium oxidation. Proc Natl Acad Sci USA. 2005;102:6478–83.CAS
PubMed
PubMed Central
Google Scholar
67.Wright JJ, Konwar KM, Hallam SJ. Microbial ecology of expanding oxygen minimum zones. Nat Rev Microbiol. 2012;10:381–94.CAS
PubMed
Google Scholar
68.Rossel PE, Stubbins A, Hach PF, Dittmar T. Bioavailability and molecular composition of dissolved organic matter from a diffuse hydrothermal system. Mar Chem. 2015;177:257–66.CAS
Google Scholar
69.Schmidt F, Koch BP, Goldhammer T, Elvert M, Witt M, Lin Y, et al. Unraveling signatures of biogeochemical processes and the depositional setting in the molecular composition of pore water DOM across different marine environments. Geochim Cosmochim Acta. 2017;207:57–80.CAS
Google Scholar
70.Gruninger RJ, Puniya AK, Callaghan TM, Edwards JE, Youssef N, Dagar SS, et al. Anaerobic fungi (phylum Neocallimastigomycota): advances in understanding their taxonomy, life cycle, ecology, role and biotechnological potential. FEMS Microbiol Ecol. 2014;90:1–17.CAS
PubMed
Google Scholar
71.Jones MD, Richards TA, Hawksworth DL, Bass D. Validation and justification of the phylum name Cryptomycota phyl. nov. IMA Fungus. 2011;2:173–5.PubMed
PubMed Central
Google Scholar
72.Spatafora JW, Chang Y, Benny GL, Lazarus K, Smith ME, Berbee ML, et al. A phylum-level phylogenetic classification of zygomycete fungi based on genome-scale data. Mycologia. 2016;108:1028–46.CAS
PubMed
PubMed Central
Google Scholar
73.Morand SC, Bertignac M, Iltis A, Kolder ICRM, Pirovano W, Jourdain R, et al. Complete genome sequence of Malassezia restricta CBS 7877, an opportunist pathogen involved in dandruff and seborrheic dermatitis. Microbiol Resour Announc. 2019;8:e01543–18.PubMed
PubMed Central
Google Scholar
74.Buckley DH, Huangyutitham V, Hsu SF, Nelson TA. Stable isotope probing with 15N achieved by disentangling the effects of genome G+C content and isotope enrichment on DNA density. Appl Environ Microbiol. 2007;73:3189–95.CAS
PubMed
PubMed Central
Google Scholar
75.Tedersoo L, Sanchez-Ramirez S, Kõljalg U, Bahram M, Döring M, Schigel D, et al. High-level classification of the Fungi and a tool for evolutionary ecological analyses. Fungal Diversity. 2018;90:135–59.
Google Scholar
76.Walsh EA, Kirkpatrick JB, Rutherford SD, Smith DC, Sogin M, D’Hondt S, et al. Bacterial diversity and community composition from seasurface to subseafloor. ISME J. 2016;10:979–89.PubMed
Google Scholar
77.Karpov SA, Mamkaeva MA, Aleoshin VV, Nassonova E, Lilje O, Gleason FH. Morphology, phylogeny, and ecology of the aphelids (Aphelidea, Opisthokonta) and proposal for the new superphylum Opisthosporidia. Front Microbiol. 2014;5:112.PubMed
PubMed Central
Google Scholar
78.Jones MD, Forn I, Gadelha C, Egan MJ, Bass D, Massana R, et al. Discovery of novel intermediate forms redefines the fungal tree of life. Nature. 2011;474:200–3.CAS
PubMed
Google Scholar
79.Chang Y, Wang S, Sekimoto S, Aerts AL, Choi C, Clum A, et al. Phylogenomic analyses indicate that early Fungi evolved digesting cell walls of algal ancestors of land plants. Genome Biol Evol. 2015;7:1590–601.CAS
PubMed
PubMed Central
Google Scholar
80.Loron CC, Francois C, Rainbird RH, Turner EC, Borensztajn S, Javaux EJ. Early fungi from the Proterozoic era in Arctic Canada. Nature. 2019;570:232–5.CAS
PubMed
Google Scholar
81.Lyons TW, Reinhard CT, Planavsky NJ. The rise of oxygen in Earth’s early ocean and atmosphere. Nature. 2014;506:307–15.CAS
PubMed
Google Scholar
82.Passow U. Production of transparent exopolymer particles (TEP) by phyto- and bacterioplankton. Mar Ecol Prog Ser. 2002;236:1–12.
Google Scholar
83.Takahashi E, Ledauphin J, Goux D, Orvain F. Optimising extraction of extracellular polymeric substances (EPS) from benthic diatoms: comparison of the efficiency of six EPS extraction methods. Mar Freshw Res. 2009;60:1201–10.CAS
Google Scholar
84.de Brouwer JFC, Wolfstein K, Stal J. Physical characterization and diel dynamics of different fractions of extracellular polysaccharides in an axenic culture of a benthic diatom. Eur J Phycol. 2002;37:37–44.
Google Scholar
85.Bass D, Howe A, Brown N, Barton H, Demidova M, Michelle H, et al. Yeast forms dominate fungal diversity in the deep oceans. Proc R Soc B. 2007;274:3069–77.CAS
PubMed
PubMed Central
Google Scholar
86.Amend A. From dandruff to deep-sea vents: Malassezia-like fungi are ecologically hyper-diverse. PLoS Pathog. 2014;10:e1004277.PubMed
PubMed Central
Google Scholar
87.Meeboon J, Takamatsu S. Microidium phyllanthi-reticulati sp. nov. on Phyllanthus reticulatus. Mycotaxon. 2017;132:289–97.
Google Scholar
88.Lueders T, Wagner B, Claus P, Friedrich MW. Stable isotope probing of rRNA and DNA reveals a dynamic methylotroph community and trophic interactions with fungi and protozoa in oxic rice field soil. Environ Microbiol. 2004;6:60–72.CAS
PubMed
Google Scholar
89.Kjeldsen KU, Schreiber L, Thorup CA, Boesen T, Bjerg JT, Yang T, et al. On the evolution and physiology of cable bacteria. Proc Natl Acad Sci USA. 2019;116:19116–25.CAS
PubMed
PubMed Central
Google Scholar
90.Dyksma S, Bischof K, Fuchs BM, Hoffmann K, Meier D, Meyerdierks A, et al. Ubiquitous Gammaproteobacteria dominate dark carbon fixation in coastal sediments. ISME J. 2016;10:1939–53.CAS
PubMed
PubMed Central
Google Scholar
91.Middelburg JJ. Chemoautotrophy in the ocean. Geophys Res Let. 2011;38:94–97.
Google Scholar
92.Starzynska-Janiszewska A, Dulinski R, Stodolak B. Fermentation with edible Rhizopus strains to enhance the bioactive potential of hull-less pumpkin oil cake. Molecules. 2020;25:5782.CAS
PubMed Central
Google Scholar
93.Dubovenko AG, Dunaevsky YE, Belozersky MA, Oppert B, Lord JC, Elpidina EN. Trypsin-like proteins of the fungi as possible markers of pathogenicity. Fungal Biol. 2010;114:151–9.CAS
PubMed
Google Scholar
94.Arnosti C, Wietz M, Brinkhoff T, Hehemann JH, Probandt D, Zeugner L, et al. The biogeochemistry of marine polysaccharides: sources, inventories, and bacterial drivers of the carbohydrate cycle. Ann Rev Mar Sci. 2021;13:81–108.CAS
PubMed
Google Scholar
95.Rossel PE, Bienhold C, Hehemann JH, Dittmar T, Boetius A. Molecular composition of dissolved organic matter in sediment porewater of the arctic deep-sea observatory HAUSGARTEN (Fram Strait). Front Mar Sci. 2020;7:428.
Google Scholar
96.Fenchel T, Finlay BJ. Ecology and evolution in anoxic worlds. In: RM May, PH Harvey, editors. Oxford Series in Ecology and Evolution. Oxford University Press, Oxford; 1–288, 1995.97.Lynd LR, Weimer PJ, van Zyl WH, Pretorius IS. Microbial cellulose utilization: fundamentals and biotechnology. Microbiol Mol Biol Rev. 2002;66:506–77.CAS
PubMed
PubMed Central
Google Scholar More