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Microbial metabolisms in an abyssal ferromanganese crust from the Takuyo-Daigo Seamount as revealed by metagenomics


Autoři: Shingo Kato aff001;  Miho Hirai aff003;  Moriya Ohkuma aff002;  Katsuhiko Suzuki aff001
Působiště autorů: Submarine Resources Research Center, Japan Agency for Marine-Earth Science and Technology (JAMSTEC), Yokosuka, Kanagawa, Japan aff001;  Japan Collection of Microorganisms (JCM), RIKEN BioResource Research Center, Tsukuba, Ibaraki, Japan aff002;  Research and Development Center for Marine Biosciences, JAMSTEC, Yokosuka, Kanagawa, Japan aff003
Vyšlo v časopise: PLoS ONE 14(11)
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pone.0224888

Souhrn

Rocky outcrops covered with thick Fe and Mn oxide coatings, which are known as ferromanganese (Fe-Mn) crusts, are commonly found on slopes of aged seamounts in bathyal and abyssal zones. Although the presence of diverse microorganisms on these Fe-Mn crusts has been reported, little is known about their metabolism. Here, we report the metabolic potential of the microbial community in an abyssal crust collected in the Takuyo-Daigo Seamount, in the north-western Pacific. We performed shotgun metagenomic sequencing of the Fe-Mn crust, and detected putative genes involved in dissolution and precipitation of Fe and Mn, nitrification, sulfur oxidation, carbon fixation, and decomposition of organics in the metagenome. In addition, four metagenome-assembled genomes (MAGs) of abundant members in the microbial community were recovered from the metagenome. The MAGs were affiliated with Thaumarchaeota, Alphaproteobacteria, and Gammaproteobacteria, and were distantly related to previously reported genomes/MAGs of cultured and uncultured species. Putative genes involved in the above reactions were also found in the crust MAGs. Our results suggest that crust microbial communities play a role in biogeochemical cycling of C, N, S, Fe, and Mn, and imply that they contribute to the growth of Fe-Mn crusts.

Klíčová slova:

Ammonia – Coatings – Manganese – Metagenomics – Oxidation – Phylogenetic analysis – Ribosomal RNA – Sulfur


Zdroje

1. Glasby G. Manganese: Predominant role of nodules and crusts. In: Schulz H, Zabel M, editors. Marine geochemistry: Springer Berlin Heidelberg; 2006. p. 371–427.

2. Usui A, Nishi K, Sato H, Nakasato Y, Thornton B, Kashiwabara T, et al. Continuous growth of hydrogenetic ferromanganese crusts since 17Myr ago on Takuyo-Daigo Seamount, NW Pacific, at water depths of 800–5500m. Ore Geol Rev. 2017;87:71–87. http://dx.doi.org/10.1016/j.oregeorev.2016.09.032.

3. Koschinsky A, Hein J. Marine ferromanganese encrustations: Archives of changing oceans. Elements. 2017;13(3):177–82. doi: 10.2113/gselements.13.3.177

4. Goto KT, Anbar AD, Gordon GW, Romaniello SJ, Shimoda G, Takaya Y, et al. Uranium isotope systematics of ferromanganese crusts in the pacific ocean: Implications for the marine 238U/235U isotope system. Geochim Cosmochim Acta. 2014;146:43–58. http://dx.doi.org/10.1016/j.gca.2014.10.003.

5. Koschinsky A, Halbach P. Sequential leaching of marine ferromanganese precipitates: Genetic implications. Geochim Cosmochim Acta. 1995;59(24):5113–32. http://dx.doi.org/10.1016/0016-7037(95)00358-4.

6. Kashiwabara T, Oishi Y, Sakaguchi A, Sugiyama T, Usui A, Takahashi Y. Chemical processes for the extreme enrichment of tellurium into marine ferromanganese oxides. Geochim Cosmochim Acta. 2014;131(0):150–63. http://dx.doi.org/10.1016/j.gca.2014.01.020.

7. Goldberg ED. Marine geochemistry 1. Chemical scavengers of the sea. J Geol. 1954;62(3):249–65.

8. Hein JR, Koschinsky A. Deep-ocean ferromanganese crusts and nodules. In: Turekian KK, editor. Treatise on geochemistry (second edition). 13. Oxford: Elsevier; 2014. p. 273–91.

9. Shiraishi F, Mitsunobu S, Suzuki K, Hoshino T, Morono Y, Inagaki F. Dense microbial community on a ferromanganese nodule from the ultra-oligotrophic South Pacific Gyre: Implications for biogeochemical cycles. Earth Planet Sci Lett. 2016;447:10–20. doi: 10.1016/j.epsl.2016.04.021

10. Lindh MV, Maillot BM, Shulse CN, Gooday AJ, Amon DJ, Smith CR, et al. From the surface to the deep-sea: Bacterial distributions across polymetallic nodule fields in the Clarion-Clipperton Zone of the pacific ocean. Front Microbiol. 2017;8:1696. doi: 10.3389/fmicb.2017.01696 28943866

11. Nitahara S, Kato S, Usui A, Urabe T, Suzuki K, Yamagishi A. Archaeal and bacterial communities in deep-sea hydrogenetic ferromanganese crusts on old seamounts of the northwestern Pacific. PLOS ONE. 2017;12(2):e0173071. doi: 10.1371/journal.pone.0173071 28235095

12. Shulse CN, Maillot B, Smith CR, Church MJ. Polymetallic nodules, sediments, and deep waters in the equatorial north pacific exhibit highly diverse and distinct bacterial, archaeal, and microeukaryotic communities. MicrobiologyOpen. 2017;6(2):e428. doi: 10.1002/mbo3.428 27868387

13. Kato S, Okumura T, Uematsu K, Hirai M, Iijima K, Usui A, et al. Heterogeneity of microbial communities on deep-sea ferromanganese crusts in the Takuyo-Daigo Seamount. Microbes Environ. 2018;33:366–377. doi: 10.1264/jsme2.ME18090 30381615

14. Nitahara S, Kato S, Urabe T, Usui A, Yamagishi A. Molecular characterization of the microbial community in hydrogenetic ferromanganese crusts of the Takuyo-Daigo Seamount, northwest pacific. FEMS Microbiol Lett. 2011;321(2):121–9. doi: 10.1111/j.1574-6968.2011.02323.x 21631576

15. Ehrlich HL. How microbes influence mineral growth and dissolution. Chemical Geology. 1996;132(1–4):5–9.

16. Melton ED, Swanner ED, Behrens S, Schmidt C, Kappler A. The interplay of microbially mediated and abiotic reactions in the biogeochemical fe cycle. Nat Rev Micro. 2014;12(12):797–808. doi: 10.1038/nrmicro3347 25329406

17. Tebo BM, Bargar JR, Clement BG, Dick GJ, Murray KJ, Parker D, et al. Biogenic manganese oxides: Properties and mechanisms of formation. Annu Rev Earth Planet Sci. 2004;32(1):287–328. doi: 10.1146/annurev.earth.32.101802.120213

18. Tully BJ, Heidelberg JF. Microbial communities associated with ferromanganese nodules and the surrounding sediments. Front Microbiol. 2013;4:161. doi: 10.3389/fmicb.2013.00161 23805131

19. Blothe M, Wegorzewski A, Muller C, Simon F, Kuhn T, Schippers A. Manganese-cycling microbial communities inside deep-sea manganese nodules. Environ Sci Technol. 2015;49(13):7692–700. doi: 10.1021/es504930v 26020127

20. Lee MD, Walworth NG, Sylvan JB, Edwards KJ, Orcutt BN. Microbial communities on seafloor basalts at Dorado Outcrop reflect level of alteration and highlight global lithic clades. Front Microbiol. 2015;6:1470. doi: 10.3389/fmicb.2015.01470 26779122

21. DeLong E. Archaea in coastal marine environments. Proc Natl Acad Sci USA. 1992;89:5685–9. doi: 10.1073/pnas.89.12.5685 1608980

22. Könneke M, Bernhard AE, de la Torre JR, Walker CB, Waterbury JB, Stahl DA. Isolation of an autotrophic ammonia-oxidizing marine archaeon. Nature. 2005;437(7058):543–6. doi: 10.1038/nature03911 16177789

23. Nakanishi M, Tamaki K, Kobayashi K. Mesozoic magnetic anomaly lineations and seafloor spreading history of the northwestern Pacific. J Geophys Res-Solid Earth. 1989;94(B11):15437–62. doi: 10.1029/JB094iB11p15437

24. Müller RD, Sdrolias M, Gaina C, Roest WR. Age, spreading rates, and spreading asymmetry of the world's ocean crust. Geochem Geophys Geosyst. 2008;9(4):Q04006, doi: 10.1029/2007GC001743

25. DeLong EF, Preston CM, Mincer T, Rich V, Hallam SJ, Frigaard N-U, et al. Community genomics among stratified microbial assemblages in the ocean's interior. Science. 2006;311(5760):496–503. doi: 10.1126/science.1120250 16439655

26. Eloe EA, Fadrosh DW, Novotny M, Zeigler Allen L, Kim M, Lombardo MJ, et al. Going deeper: Metagenome of a hadopelagic microbial community. PLoS One. 2011;6(5):e20388. doi: 10.1371/journal.pone.0020388 21629664

27. Martin-Cuadrado AB, Lopez-Garcia P, Alba JC, Moreira D, Monticelli L, Strittmatter A, et al. Metagenomics of the deep mediterranean, a warm bathypelagic habitat. PLoS One. 2007;2(9):e914. doi: 10.1371/journal.pone.0000914 17878949

28. Konstantinidis KT, Braff J, Karl DM, DeLong EF. Comparative metagenomic analysis of a microbial community residing at a depth of 4,000 meters at station aloha in the north pacific subtropical gyre. Applied and Environmental Microbiology. 2009;75(16):5345–55. doi: 10.1128/AEM.00473-09 19542347

29. Tully BJ, Heidelberg JF. Potential mechanisms for microbial energy acquisition in oxic deep-sea sediments. Applied and Environmental Microbiology. 2016;82(14):4232–43. doi: 10.1128/AEM.01023-16 27208118

30. Reese BK, Zinke LA, Sobol MS, LaRowe DE, Orcutt BN, Zhang X, et al. Nitrogen cycling of active bacteria within oligotrophic sediment of the Mid-Atlantic Ridge flank. Geomicrobiology Journal. 2018;35(6):468–83. doi: 10.1080/01490451.2017.1392649

31. Singer E, Chong L, Heidelberg J, Edwards K. Similar microbial communities found on two distant seafloor basalts. Frontiers in Microbiology. 2015;6. doi: 10.3389/fmicb.2015.01409 26733957

32. Hirai M, Nishi S, Tsuda M, Sunamura M, Takaki Y, Nunoura T. Library construction from subnanogram DNA for pelagic sea water and deep-sea sediments. Microbes Environ. 2017;32(4):336–43. doi: 10.1264/jsme2.ME17132 29187708

33. Kato S, Shibuya T, Takaki Y, Hirai M, Nunoura T, Suzuki K. Genome-enabled metabolic reconstruction of dominant chemosynthetic colonizers in deep-sea massive sulfide deposits. Environ Microbiol. 2018;20(2):862–77. doi: 10.1111/1462-2920.14032 29322618

34. Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M, Kulikov AS, et al. SPAdes: A new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol. 2012;19(5):455–77. doi: 10.1089/cmb.2012.0021 22506599

35. Hyatt D, Chen GL, Locascio PF, Land ML, Larimer FW, Hauser LJ. Prodigal: Prokaryotic gene recognition and translation initiation site identification. BMC Bioinformatics. 2010;11(1):119. doi: 10.1186/1471-2105-11-119 20211023

36. Ogata H, Goto S, Sato K, Fujibuchi W, Bono H, Kanehisa M. KEGG: Kyoto encyclopedia of genes and genomes. Nucleic Acids Res. 1999;27(1):29–34. doi: 10.1093/nar/27.1.29 9847135

37. Kanehisa M, Sato Y, Morishima K. BlastKOALA and GhostKOALA: KEGG tools for functional characterization of genome and metagenome sequences. J MolBiol. 2016;428(4):726–31. doi: 10.1016/j.jmb.2015.11.006 26585406

38. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, et al. Gapped BLAST and PSI-BLAST: A new generation of protein database search programs. Nucleic Acids Res. 1997;25(17):3389–402. doi: 10.1093/nar/25.17.3389 9254694

39. Huson DH, Beier S, Flade I, Górska A, El-Hadidi M, Mitra S, et al. MEGAN community edition—interactive exploration and analysis of large-scale microbiome sequencing data. PLoS Comput Biol. 2016;12(6):e1004957. doi: 10.1371/journal.pcbi.1004957 27327495

40. Huson DH, Auch AF, Qi J, Schuster SC. MEGAN analysis of metagenomic data. Genome Res. 2007;17(3):377–86. doi: 10.1101/gr.5969107 17255551

41. Gruber-Vodicka HR, Seah BKB, Pruesse E. phyloFlash—rapid SSU rRNA profiling and targeted assembly from metagenomes. bioRxiv. 2019:521922. doi: 10.1101/521922

42. Lombard V, Golaconda Ramulu H, Drula E, Coutinho PM, Henrissat B. The carbohydrate-active enzymes database (cazy) in 2013. Nucleic Acids Research. 2014;42(D1):D490–D5. doi: 10.1093/nar/gkt1178 24270786

43. Zhang H, Yohe T, Huang L, Entwistle S, Wu P, Yang Z, et al. Dbcan2: A meta server for automated carbohydrate-active enzyme annotation. Nucleic Acids Research. 2018;46(W1):W95–W101. doi: 10.1093/nar/gky418 29771380

44. Eddy SR. Accelerated profile hmm searches. PLOS Computational Biology. 2011;7(10):e1002195. doi: 10.1371/journal.pcbi.1002195 22039361

45. Kang DD, Froula J, Egan R, Wang Z. MetaBAT, an efficient tool for accurately reconstructing single genomes from complex microbial communities. PeerJ. 2015;3:e1165. doi: 10.7717/peerj.1165 26336640

46. Seah BKB, Gruber-Vodicka HR. gbtools: Interactive visualization of metagenome bins in R. Front Microbiol. 2015;6: doi: 10.3389/fmicb.2015.01451 26732662

47. Seemann T. Prokka: Rapid prokaryotic genome annotation. Bioinformatics. 2014;30(14):2068–9. doi: 10.1093/bioinformatics/btu153 24642063

48. Rodriguez R LM, Konstantinidis KT. The enveomics collection: A toolbox for specialized analyses of microbial genomes and metagenomes. PeerJ Preprints. 2016;4:e1900v1. doi: 10.7287/peerj.preprints.1900v1

49. Parks DH, Imelfort M, Skennerton CT, Hugenholtz P, Tyson GW. CheckM: Assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes. Genome Res. 2015;25(7):1043–55. doi: 10.1101/gr.186072.114 25977477

50. Edgar RC. MUSCLE: Multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 2004;32(5):1792–7. doi: 10.1093/nar/gkh340 15034147

51. Capella-Gutierrez S, Silla-Martinez JM, Gabaldon T. trimAl: A tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics. 2009;25(15):1972–3. doi: 10.1093/bioinformatics/btp348 19505945

52. Stamatakis A. RAxML version 8: A tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics. 2014;30(9):1312–3. doi: 10.1093/bioinformatics/btu033 24451623

53. Baker BJ, Lazar CS, Teske AP, Dick GJ. Genomic resolution of linkages in carbon, nitrogen, and sulfur cycling among widespread estuary sediment bacteria. Microbiome. 2015;3(1):14. doi: 10.1186/s40168-015-0077-6 25922666

54. Daims H, Lebedeva EV, Pjevac P, Han P, Herbold C, Albertsen M, et al. Complete nitrification by Nitrospira bacteria. Nature. 2015;528(7583):504–9. doi: 10.1038/nature16461 26610024

55. van Kessel MA, Speth DR, Albertsen M, Nielsen PH, Op den Camp HJ, Kartal B, et al. Complete nitrification by a single microorganism. Nature. 2015;528(7583):555–9. doi: 10.1038/nature16459 26610025

56. Pester M, Maixner F, Berry D, Rattei T, Koch H, Lucker S, et al. NxrB encoding the beta subunit of nitrite oxidoreductase as functional and phylogenetic marker for nitrite-oxidizing Nitrospira. Environ Microbiol. 2014;16(10):3055–71. doi: 10.1111/1462-2920.12300 24118804

57. Hügler M, Sievert SM. Beyond the calvin cycle: Autotrophic carbon fixation in the ocean. Annual Review of Marine Science. 2010;3(1):261–89. doi: 10.1146/annurev-marine-120709-142712 21329206

58. Sunda WG, Kieber DJ. Oxidation of humic substances by manganese oxides yields low-molecular-weight organic substrates. Nature. 1994;367(6458):62–4.

59. Myers JM, Myers CR. Role for outer membrane cytochromes omca and omcb of shewanella putrefaciens mr-1 in reduction of manganese dioxide. Applied and Environmental Microbiology. 2001;67(1):260–9. doi: 10.1128/AEM.67.1.260-269.2001 11133454

60. Mehta T, Coppi MV, Childers SE, Lovley DR. Outer membrane c-type cytochromes required for Fe(III) and Mn(IV) oxide reduction in Geobacter sulfurreducens. Appl Environ Microbiol. 2005;71(12):8634–41. doi: 10.1128/AEM.71.12.8634-8641.2005 16332857

61. Leang C, Coppi MV, Lovley DR. Omcb, a c-type polyheme cytochrome, involved in Fe(III) reduction in Geobacter sulfurreducens. J Bacteriol. 2003;185. doi: 10.1128/JB.185.7.2096–2103.2003

62. Butler JE, Young ND, Lovley DR. Evolution of electron transfer out of the cell: Comparative genomics of six Geobacter genomes. BMC Genomics. 2010;11(1):40. doi: 10.1186/1471-2164-11-40 20078895

63. Kato S, Ohkuma M, Powell DH, Krepski ST, Oshima K, Hattori M, et al. Comparative genomic insights into ecophysiology of neutrophilic, microaerophilic iron oxidizing bacteria. Front Microbiol. 2015;6: doi: 10.3389/fmicb.2015.01265 26617599

64. Barco RA, Emerson D, Sylvan JB, Orcutt BN, Jacobson Meyers ME, Ramirez GA, et al. New insight into microbial iron oxidation as revealed by the proteomic profile of an obligate iron-oxidizing chemolithoautotroph. Appl Environ Microbiol. 2015;81(17):5927–37. doi: 10.1128/AEM.01374-15 26092463

65. Castelle C, Guiral M, Malarte G, Ledgham F, Leroy G, Brugna M, et al. A new iron-oxidizing/O2-reducing supercomplex spanning both inner and outer membranes, isolated from the extreme acidophile Acidithiobacillus ferrooxidans. J Biol Chem. 2008;283(38):25803–11. doi: 10.1074/jbc.M802496200 18632666

66. Emerson D, Rentz JA, Lilburn TG, Davis RE, Aldrich H, Chan C, et al. A novel lineage of proteobacteria involved in formation of marine fe-oxidizing microbial mat communities. PLOS ONE. 2007;2(8):e667. doi: 10.1371/journal.pone.0000667 17668050

67. Kato S, Krepski S, Chan C, Itoh T, Ohkuma M. Ferriphaselus amnicola gen. nov., sp. nov., a neutrophilic, stalk-forming, iron-oxidizing bacterium isolated from an iron-rich groundwater seep. Int J Syst Evol Microbiol. 2014;64(Pt 3):921–5. doi: 10.1099/ijs.0.058487-0 24425821

68. Geszvain K, Butterfield C, Davis Richard E, Madison Andrew S, Lee S-W, Parker Dorothy L, et al. The molecular biogeochemistry of manganese(II) oxidation. Biochemical Society Transactions. 2012;40(6):1244–8. doi: 10.1042/BST20120229 23176462

69. Tebo BM, Johnson HA, McCarthy JK, Templeton AS. Geomicrobiology of manganese(II) oxidation. Trends Microbiol. 2005;13(9):421–8. doi: 10.1016/j.tim.2005.07.009 16054815

70. Anderson CR, Johnson HA, Caputo N, Davis RE, Torpey JW, Tebo BM. Mn(II) oxidation is catalyzed by heme peroxidases in “aurantimonas manganoxydans” strain si85-9a1 and erythrobacter sp. Strain sd-21. Applied and Environmental Microbiology. 2009;75(12):4130–8. doi: 10.1128/AEM.02890-08 19411418

71. Andeer PF, Learman DR, McIlvin M, Dunn JA, Hansel CM. Extracellular haem peroxidases mediate Mn(II) oxidation in a marine roseobacter bacterium via superoxide production. Environmental Microbiology. 2015;17(10):3925–36. doi: 10.1111/1462-2920.12893 25923595

72. Learman DR, Voelker BM, Madden AS, Hansel CM. Constraints on superoxide mediated formation of manganese oxides. Front Microbiol. 2013;4:262. doi: 10.3389/fmicb.2013.00262 24027565

73. Bowers RM, Kyrpides NC, Stepanauskas R, Harmon-Smith M, Doud D, Reddy TBK, et al. Minimum information about a single amplified genome (MISAG) and a metagenome-assembled genome (MIMAG) of bacteria and archaea. Nat Biotechnol. 2017;35(8):725–31. doi: 10.1038/nbt.3893 28787424

74. Qin W, Heal KR, Ramdasi R, Kobelt JN, Martens-Habbena W, Bertagnolli AD, et al. Nitrosopumilus maritimus gen. nov., sp. nov., nitrosopumilus cobalaminigenes sp. nov., nitrosopumilus oxyclinae sp. nov., and nitrosopumilus ureiphilus sp. nov., four marine ammonia-oxidizing archaea of the phylum Thaumarchaeota. Int J Syst Evol Microbiol. 2017;67:5067–79. doi: 10.1099/ijsem.0.002416 29034851

75. Santoro AE, Dupont CL, Richter RA, Craig MT, Carini P, McIlvin MR, et al. Genomic and proteomic characterization of “Candidatus nitrosopelagicus brevis”: An ammonia-oxidizing archaeon from the open ocean. Proceedings of the National Academy of Sciences. 2015;112(4):1173–8. doi: 10.1073/pnas.1416223112 25587132

76. Konstantinidis KT, Rossello-Mora R, Amann R. Uncultivated microbes in need of their own taxonomy. ISME J. 2017;11(11):2399–406. doi: 10.1038/ismej.2017.113 28731467

77. Yarza P, Yilmaz P, Pruesse E, Glockner FO, Ludwig W, Schleifer K-H, et al. Uniting the classification of cultured and uncultured bacteria and archaea using 16S rRNA gene sequences. Nat Rev Micro. 2014;12(9):635–45. doi: 10.1038/nrmicro3330 http://www.nature.com/nrmicro/journal/v12/n9/abs/nrmicro3330.html - supplementary-information. 25118885

78. Walker CB, de la Torre JR, Klotz MG, Urakawa H, Pinel N, Arp DJ, et al. Nitrosopumilus maritimus genome reveals unique mechanisms for nitrification and autotrophy in globally distributed marine crenarchaea. Proc Natl Acad Sci USA. 2010;107(19):8818–23. doi: 10.1073/pnas.0913533107 20421470

79. Kerou M, Offre P, Valledor L, Abby SS, Melcher M, Nagler M, et al. Proteomics and comparative genomics of nitrososphaera viennensis reveal the core genome and adaptations of archaeal ammonia oxidizers. Proc Natl Acad Sci USA. 2016;113(49):E7937–E46. doi: 10.1073/pnas.1601212113 27864514

80. Lehtovirta-Morley LE, Sayavedra-Soto LA, Gallois N, Schouten S, Stein LY, Prosser JI, et al. Identifying potential mechanisms enabling acidophily in the ammonia-oxidizing archaeon “Candidatus nitrosotalea devanaterra”. Applied and Environmental Microbiology. 2016;82(9):2608–19. doi: 10.1128/AEM.04031-15 26896134

81. Mosier AC, Lund MB, Francis CA. Ecophysiology of an ammonia-oxidizing archaeon adapted to low-salinity habitats. Microbial Ecology. 2012;64(4):955–63. doi: 10.1007/s00248-012-0075-1 22644483

82. Lassak K, Ghosh A, Albers S-V. Diversity, assembly and regulation of archaeal type IV pili-like and non-type-IV pili-like surface structures. Research in Microbiology. 2012;163(9):630–44. https://doi.org/10.1016/j.resmic.2012.10.024.

83. Anantharaman K, Brown CT, Hug LA, Sharon I, Castelle CJ, Probst AJ, et al. Thousands of microbial genomes shed light on interconnected biogeochemical processes in an aquifer system. Nat Commun. 2016;7:13219. doi: 10.1038/ncomms13219 http://www.nature.com/articles/ncomms13219-supplementary-information.27774985

84. Bienhold C, Zinger L, Boetius A, Ramette A. Diversity and biogeography of bathyal and abyssal seafloor bacteria. PLOS ONE. 2016;11(1):e0148016. doi: 10.1371/journal.pone.0148016 26814838

85. Mußmann M, Pjevac P, Krüger K, Dyksma S. Genomic repertoire of the woeseiaceae/jtb255, cosmopolitan and abundant core members of microbial communities in marine sediments. ISME J. 2017;11(5):1276–81. doi: 10.1038/ismej.2016.185 28060363

86. Du Z-J, Wang Z-J, Zhao J-X, Chen G-J. Woeseia oceani gen. nov., sp. nov., a chemoheterotrophic member of the order chromatiales, and proposal of woeseiaceae fam. Nov. International Journal of Systematic and Evolutionary Microbiology. 2016;66(1):107–12. doi: 10.1099/ijsem.0.000683 26474827

87. 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(8):1939–53. doi: 10.1038/ismej.2015.257 26872043

88. Rees AP, Woodward EMS, Joint I. Concentrations and uptake of nitrate and ammonium in the atlantic ocean between 60on and 50os. Deep Sea Research Part II: Topical Studies in Oceanography. 2006;53(14–16):1649–65.

89. Wuchter C, Abbas B, Coolen MJ, Herfort L, van Bleijswijk J, Timmers P, et al. Archaeal nitrification in the ocean. Proc Natl Acad Sci U S A. 2006;103(33):12317–22. doi: 10.1073/pnas.0600756103 16894176

90. Tolar BB, Wallsgrove NJ, Popp BN, Hollibaugh JT. Oxidation of urea-derived nitrogen by thaumarchaeota-dominated marine nitrifying communities. Environmental Microbiology. 2017;19(12):4838–50. doi: 10.1111/1462-2920.13457 27422798

91. Alonso-Sáez L, Waller AS, Mende DR, Bakker K, Farnelid H, Yager PL, et al. Role for urea in nitrification by polar marine archaea. Proc Natl Acad Sci U S A. 2012;109(44):17989–94. doi: 10.1073/pnas.1201914109 23027926

92. Kitzinger K, Padilla CC, Marchant HK, Hach PF, Herbold CW, Kidane AT, et al. Cyanate and urea are substrates for nitrification by Thaumarchaeota in the marine environment. Nature Microbiology. 2019;4(2):234–43. doi: 10.1038/s41564-018-0316-2 30531977

93. Qin W, Amin SA, Martens-Habbena W, Walker CB, Urakawa H, Devol AH, et al. Marine ammonia-oxidizing archaeal isolates display obligate mixotrophy and wide ecotypic variation. Proc Natl Acad Sci U S A. 2014;111(34):12504–9. doi: 10.1073/pnas.1324115111 25114236

94. Bayer B, Vojvoda J, Offre P, Alves RJ, Elisabeth NH, Garcia JA, et al. Physiological and genomic characterization of two novel marine thaumarchaeal strains indicates niche differentiation. ISME J. 2016;10(5):1051–63. doi: 10.1038/ismej.2015.200 26528837

95. Palatinszky M, Herbold C, Jehmlich N, Pogoda M, Han P, von Bergen M, et al. Cyanate as an energy source for nitrifiers. Nature. 2015;524:105. doi: 10.1038/nature14856 https://www.nature.com/articles/nature14856 - supplementary-information. 26222031

96. Widner B, Mulholland MR, Mopper K. Chromatographic determination of nanomolar cyanate concentrations in estuarine and sea waters by precolumn fluorescence derivatization. Anal Chem. 2013;85(14):6661–6. doi: 10.1021/ac400351c 23738747

97. Hansell DA. Recalcitrant dissolved organic carbon fractions. Annu Rev Mar Sci. 2013;5(1):421–45. doi: 10.1146/annurev-marine-120710-100757 22881353

98. Barber RT. Dissolved organic carbon from deep waters resists microbial oxidation. Nature. 1968;220(5164):274–5. doi: 10.1038/220274a0 5684857

99. Learman DR, Voelker BM, Vazquez-Rodriguez AI, Hansel CM. Formation of manganese oxides by bacterially generated superoxide. Nat Geosci. 2011;4(2):95–8. doi: 10.1038/Ngeo1055

100. Moreau JW, Weber PK, Martin MC, Gilbert B, Hutcheon ID, Banfield JF. Extracellular proteins limit the dispersal of biogenic nanoparticles. Science. 2007;316(5831):1600–3. doi: 10.1126/science.1141064 17569859

101. Kleber M, Eusterhues K, Keiluweit M, Mikutta C, Mikutta R, Nico PS. Mineral–organic associations: Formation, properties, and relevance in soil environments. In: Sparks DL, editor. Advances in agronomy. 130: Academic Press; 2015. p. 1–140.


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