Catabolic protein degradation in marine sediments confined to distinct archaea
Castelle CJ, Banfield JF. Major new microbial groups expand diversity and alter our understanding of the tree of life. Cell. 2018;172:1181–97.CAS
PubMed
Google Scholar
Hug LA, Baker BJ, Anantharaman K, Brown CT, Probst AJ, Castelle CJ, et al. A new view of the tree of life. Nat Microbiol. 2016;1:16048.CAS
PubMed
PubMed Central
Google Scholar
Parks DH, Rinke C, Chuvochina M, Chaumeil PA, Woodcroft BJ, Evans PN, et al. Recovery of nearly 8,000 metagenome-assembled genomes substantially expands the tree of life. Nat Microbiol. 2017;2:1533–42.CAS
PubMed
Google Scholar
Imachi H, Nobu MK, Nakahara N, Morono Y, Ogawara M, Takaki Y. et al. Isolation of an archaeon at the prokaryote-eukaryote interface. Nature. 2020;577:519–25.CAS
PubMed
PubMed Central
Google Scholar
Spang A, Saw JH, Jorgensen SL, Zaremba-Niedzwiedzka K, Martijn J, Lind AE. et al. Complex archaea that bridge the gap between prokaryotes and eukaryotes. Nature. 2015;521:173–9.CAS
PubMed
PubMed Central
Google Scholar
Liu Y, Makarova KS, Huang W-C, Wolf YI, Nikolskaya AN, Zhang X. et al. Expanded diversity of Asgard archaea and their relationships with eukaryotes. Nature. 2021;593:553–7.CAS
PubMed
Google Scholar
Huber H, Stetter KO Thermoplasmatales. In: M Dworkin, S Falkow, E Rosenberg, KH Schleifer, E Stackebrandt (eds). The Prokaryotes, 3rd edn. (Springer, New York, 2006), pp 101–12.Inagaki F, Suzuki M, Takai K, Oida H, Sakamoto T, Aoki K, et al. Microbial communities associated with geological horizons in coastal subseafloor sediments from the Sea of Okhotsk. Appl Environ Microbiol. 2003;69:7224–35.CAS
PubMed
PubMed Central
Google Scholar
Vetriani C, Jannasch HW, MacGregor AJ, Stahl DA, Reysenbach AR. Population structure and phylogenetic characterization of marine benthic archaea in deep-sea sediments. Appl Environ Microbiol. 1999;65:4375–84.CAS
PubMed
PubMed Central
Google Scholar
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. 2019;5:248–55.PubMed
Google Scholar
Yu T, Wu W, Liang W, Lever MA, Hinrichs KU, Wang F. Growth of sedimentary Bathyarchaeota on lignin as an energy source. Proc Natl Acad Sci USA. 2018;115:6022–7.CAS
PubMed
PubMed Central
Google Scholar
Yin X, Cai M, Liu Y, Zhou G, Richter-Heitmann T, Aromokeye DA, et al. Subgroup level differences of physiological activities in marine Lokiarchaeota. ISME J. 2020;15:848–61.PubMed
PubMed Central
Google Scholar
Lloyd KG, Schreiber L, Petersen DG, Kjeldsen KU, Lever MA, Steen AD. et al. Predominant archaea in marine sediments degrade detrital proteins. Nature. 2013;496:215–8.CAS
PubMed
Google Scholar
Lin X, Handley KM, Gilbert JA, Kostka JE. Metabolic potential of fatty acid oxidation and anaerobic respiration by abundant members of Thaumarchaeota and Thermoplasmata in deep anoxic peat. ISME J. 2015;9:2740–4.CAS
PubMed
PubMed Central
Google Scholar
He Y, Li M, Perumal V, Feng X, Fang J, Xie J, et al. Genomic and enzymatic evidence for acetogenesis among multiple lineages of the archaeal phylum Bathyarchaeota widespread in marine sediments. Nat Microbiol. 2016;1:16035.CAS
PubMed
Google Scholar
Zhou Z, Liu Y, Lloyd KG, Pan J, Yang Y, Gu J-D, et al. Genomic and transcriptomic insights into the ecology and metabolism of benthic archaeal cosmopolitan, Thermoprofundales (MBG-D archaea). ISME J. 2019;13:885–901.CAS
PubMed
Google Scholar
Lazar CS, Baker BJ, Seitz K, Hyde AS, Dick GJ, Hinrichs KU, et al. Genomic evidence for distinct carbon substrate preferences and ecological niches of Bathyarchaeota in estuarine sediments. Environ Microbiol. 2016;18:1200–11.CAS
PubMed
Google Scholar
Cai M, Liu Y, Yin X, Zhou Z, Friedrich MW, Richter-Heitmann T, et al. Diverse Asgard archaea including the novel phylum Gerdarchaeota participate in organic matter degradation. Sci China Life Sci. 2020;63:886–97.CAS
PubMed
Google Scholar
Spang A, Stairs CW, Dombrowski N, Eme L, Lombard J, Caceres EF, et al. Proposal of the reverse flow model for the origin of the eukaryotic cell based on comparative analyses of Asgard archaeal metabolism. Nat Microbiol. 2019;4:1138–48.CAS
PubMed
Google Scholar
Baker BJ, Appler KE, Gong X. New microbial biodiversity in marine sediments. Ann Rev Mar Sci. 2020;13:161–75.PubMed
Google Scholar
Gorke B, Stulke J. Carbon catabolite repression in bacteria: many ways to make the most out of nutrients. Nat Rev Microbiol. 2008;6:613–24.PubMed
Google Scholar
Siliakus MF, van der Oost J, Kengen SWM. Adaptations of archaeal and bacterial membranes to variations in temperature, pH and pressure. Extremophiles. 2017;21:651–70.CAS
PubMed
PubMed Central
Google Scholar
Takano Y, Chikaraishi Y, Ogawa NO, Nomaki H, Morono Y, Inagaki F. et al. Sedimentary membrane lipids recycled by deep-sea benthic archaea. Nat Geosci. 2010;3:858–61.CAS
Google Scholar
Li M, Baker BJ, Anantharaman K, Jain S, Breier JA, Dick GJ. Genomic and transcriptomic evidence for scavenging of diverse organic compounds by widespread deep-sea archaea. Nat Commun. 2015;6:8933.CAS
PubMed
Google Scholar
Dekas AE, Parada AE, Mayali X, Fuhrman JA, Wollard J, Weber PK, et al. Characterizing chemoautotrophy and heterotrophy in marine Archaea and Bacteria with single-cell multi-isotope NanoSIP. Front Microbiol. 2019;10:2682.PubMed
PubMed Central
Google Scholar
Vuillemin A, Wankel SD, Coskun ÖK, Magritsch T, Vargas S, Estes ER. et al. Archaea dominate oxic subseafloor communities over multimillion-year time scales. Sci Adv. 2019;5:eaaw4108PubMed
PubMed Central
Google Scholar
Könneke M, Bernhard AE, de la Torre JR, Walker CB, Waterbury JB, Stahl DA. Isolation of an autotrophic ammonia-oxidizing marine archaeon. Nature. 2005;437:543–6.PubMed
Google Scholar
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 USA. 2014;111:12504–9.CAS
PubMed
PubMed Central
Google Scholar
Aoyagi T, Hanada S, Itoh H, Sato Y, Ogata A, Friedrich MW, et al. Ultra-high-sensitivity stable-isotope probing of rRNA by high-throughput sequencing of isopycnic centrifugation gradients. Environ Microbiol Rep. 2015;7:282–7.CAS
PubMed
Google Scholar
Yin X, Wu W, Maeke M, Richter-Heitmann T, Kulkarni AC, Oni OE, et al. CO2 conversion to methane and biomass in obligate methylotrophic methanogens in marine sediments. ISME J. 2019;13:2107–19.CAS
PubMed
PubMed Central
Google Scholar
Oni O, Miyatake T, Kasten S, Richter-Heitmann T, Fischer D, Wagenknecht L, et al. Distinct microbial populations are tightly linked to the profile of dissolved iron in the methanic sediments of the Helgoland mud area, North Sea. Front Microbiol. 2015;6:365.PubMed
PubMed Central
Google Scholar
Bohrmann G, Aromokeye AD, Bihler V, Dehning K, Dohrmann I, Gentz T, et al. R/V METEOR Cruise Report M134, Emissions of free gas from cross-shelf troughs of South Georgia: distribution, quantification, and sources for methane ebullition sites in sub-Antarctic waters, Port Stanley (Falkland Islands) – Punta Arenas (Chile). Ber aus dem MARUM und dem Fachbereich Geowissenschaften der Univät Brem. 2017;317:1–220.
Google Scholar
Yin X, Kulkarni AC, Friedrich MW DNA and RNA stable isotope probing of methylotrophic methanogenic archaea. In: Dumont M, Hernández García M (eds), Stable Isotope Probing, Methods in Molecular Biology, (Humana Press New York, 2019) pp 189–206.Danovaro R, Dell¹Anno A, Fabiano M. Bioavailability of organic matter in the sediments of the Porcupine Abyssal Plain, northeastern Atlantic. Mar Ecol Prog Ser. 2001;220:25–32.CAS
Google Scholar
Yang T, Jiang S-Y, Yang J-H, Lu G, Wu N-Y, Liu J, et al. Dissolved inorganic carbon (DIC) and its carbon isotopic composition in sediment pore waters from the Shenhu area, northern South China Sea. J Oceanogr. 2008;64:303–10.CAS
Google Scholar
Lueders T, Manefield M, Friedrich MW. Enhanced sensitivity of DNA- and rRNA-based stable isotope probing by fractionation and quantitative analysis of isopycnic centrifugation gradients. Environ Microbiol. 2003;6:73–8.
Google Scholar
Ovreas L, Forney L, Daae FL, Torsvik V. Distribution of bacterioplankton in meromictic Lake Saelenvannet, as determined by denaturing gradient gel electrophoresis of PCR-amplified gene fragments coding for 16S rRNA. Appl Environ Microbiol. 1997;63:3367–73.CAS
PubMed
PubMed Central
Google Scholar
Takai K, Horikoshi K. Rapid detection and quantification of members of the archaeal community by quantitative PCR using fluorogenic probes. Appl Environ Microbiol. 2000;66:5066–72.CAS
PubMed
PubMed Central
Google Scholar
Aromokeye DA, Richter-Heitmann T, Oni OE, Kulkarni A, Yin X, Kasten S, et al. Temperature controls crystalline iron oxide utilization by microbial communities in methanic ferruginous marine sediment incubations. Front Microbiol. 2018;9:2574.PubMed
PubMed Central
Google Scholar
Edgar RC. UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods. 2013;10:996–8.CAS
Google Scholar
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:D590–6.CAS
PubMed
Google Scholar
Wegener G, Kellermann MY, Elvert M. Tracking activity and function of microorganisms by stable isotope probing of membrane lipids. Curr Opin Biotechnol. 2016;41:43–52.CAS
PubMed
Google Scholar
Boschker HTS, Nold SC, Wellsbury P, Bos D, de Graaf W, Pel R. et al. Direct linking of microbial populations to specific biogeochemical processes by 13C-labelling of biomarkers. Nature. 1998;392:801–5.CAS
Google Scholar
Sturt HF, Summons RE, Smith K, Elvert M, Hinrichs KU. Intact polar membrane lipids in prokaryotes and sediments deciphered by high-performance liquid chromatography/electrospray ionization multistage mass spectrometry-new biomarkers for biogeochemistry and microbial ecology. Rapid Commun Mass Spectrom. 2004;18:617–28.CAS
PubMed
Google Scholar
Liu XL, Lipp JS, Simpson JH, Lin YS, Summons RE, Hinrichs KU. Mono- and dihydroxyl glycerol dibiphytanyl glycerol tetraethers in marine sediments: Identification of both core and intact polar lipid forms. Geochim Cosmochim Acta. 2012;89:102–15.CAS
Google Scholar
Ertefai TF, Heuer VB, Prieto-Mollar X, Vogt C, Sylva SP, Seewald J, et al. The biogeochemistry of sorbed methane in marine sediments. Geochim Cosmochim Acta. 2010;74:6033–48.CAS
Google Scholar
Baker BJ, De Anda V, Seitz KW, Dombrowski N, Santoro AE, Lloyd KG. Diversity, ecology and evolution of Archaea. Nat Microbiol. 2020;5:887–900.CAS
PubMed
Google Scholar
Hu W, Pan J, Wang B, Guo J, Li M, Xu M. Metagenomic insights into the metabolism and evolution of a new Thermoplasmata order (Candidatus Gimiplasmatales). Environ Microbiol. 2020;23:3695–709.PubMed
Google Scholar
Spang A, Stairs CW, Dombrowski N, Eme L, Lombard J, Caceres EF, et al. Proposal of the reverse flow model for the origin of the eukaryotic cell based on comparative analyses of Asgard archaeal metabolism. Nat Microbiol. 2019;4:1138–48.CAS
PubMed
Google Scholar
Almagro Armenteros JJ, Tsirigos KD, Sonderby CK, Petersen TN, Winther O, Brunak S, et al. SignalP 5.0 improves signal peptide predictions using deep neural networks. Nat Biotechnol. 2019;37:420–3.CAS
PubMed
Google Scholar
Uritskiy GV, DiRuggiero J, Taylor J. MetaWRAP-a flexible pipeline for genome-resolved metagenomic data analysis. Microbiome. 2018;6:158PubMed
PubMed Central
Google Scholar
Li D, Luo R, Liu CM, Leung CM, Ting HF, Sadakane K. et al. MEGAHIT v1.0: A fast and scalable metagenome assembler driven by advanced methodologies and community practices. Methods. 2016;102:3–11.CAS
PubMed
Google Scholar
Wu Y-W, Simmons BA, Singer SW. MaxBin 2.0: an automated binning algorithm to recover genomes from multiple metagenomic datasets. Bioinformatics. 2015;32:605–7.PubMed
Google Scholar
Alneberg J, Bjarnason BS, de Bruijn I, Schirmer M, Quick J, Ijaz UZ, et al. Binning metagenomic contigs by coverage and composition. Nat Methods. 2014;11:1144–6.CAS
PubMed
Google Scholar
Kang DD, Li F, Kirton E, Thomas A, Egan R, An H. et al. MetaBAT 2: an adaptive binning algorithm for robust and efficient genome reconstruction from metagenome assemblies. PeerJ. 2019;7:e7359–e.PubMed
PubMed Central
Google Scholar
Li H, Durbin R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics. 2009;25:1754–60.CAS
PubMed
PubMed Central
Google Scholar
Nurk S, Meleshko D, Korobeynikov A, Pevzner PA. metaSPAdes: a new versatile metagenomic assembler. Genome Res. 2017;27:824–34.CAS
PubMed
PubMed Central
Google Scholar
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;25:1043–55.CAS
PubMed
PubMed Central
Google Scholar
Chaumeil PA, Mussig AJ, Hugenholtz P, Parks DH. GTDB-Tk: a toolkit to classify genomes with the Genome Taxonomy Database. J Bioinform. 2019;36:1925–7.
Google Scholar
Hyatt D, Chen GL, LoCascio PF, Land ML, Larimer FW, Hauser LJ. Prodigal: prokaryotic gene recognition and translation initiation site identification. BMC Bioinforma. 2010;11:119.
Google Scholar
Kanehisa M, Sato Y, Morishima K. BlastKOALA and GhostKOALA: KEGG tools for functional characterization of genome and metagenome sequences. J Mol Biol. 2016;428:726–31.CAS
PubMed
Google Scholar
Huerta-Cepas J, Forslund K, Coelho LP, Szklarczyk D, Jensen LJ, von Mering C, et al. Fast genome-wide functional annotation through orthology assignment by eggNOG-mapper. Mol Biol Evol. 2017;34:2115–22.CAS
PubMed
PubMed Central
Google Scholar
Jones P, Binns D, Chang H-Y, Fraser M, Li W, McAnulla C. et al. InterProScan 5: genome-scale protein function classification. Bioinformatics. 2014;30:1236–40.CAS
PubMed
PubMed Central
Google Scholar
Pruesse E, Peplies J, Glöckner FO. SINA: accurate high-throughput multiple sequence alignment of ribosomal RNA genes. Bioinformatics. 2012;28:1823–9.CAS
PubMed
PubMed Central
Google Scholar
Ludwig W, Strunk O, Westram R, Richter L, Meier H, Yadhukumar, et al. ARB: a software environment for sequence data. Nucleic Acids Res. 2004;32:1363–71.CAS
PubMed
PubMed Central
Google Scholar
Stamatakis A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics. 2014;30:1312–3.CAS
PubMed
PubMed Central
Google Scholar
Letunic I, Bork P. Interactive Tree Of Life (iTOL): an online tool for phylogenetic tree display and annotation. Bioinformatics. 2006;23:127–8.PubMed
Google Scholar
Zhou Z, Pan J, Wang F, Gu JD, Li M. Bathyarchaeota: globally distributed metabolic generalists in anoxic environments. FEMS Microbiol Rev. 2018;42:639–55.CAS
PubMed
Google Scholar
Lee MD. GToTree: a user-friendly workflow for phylogenomics. Bioinformatics. 2019;35:4162–4.CAS
PubMed
PubMed Central
Google Scholar
Eren AM, Esen OC, Quince C, Vineis JH, Morrison HG, Sogin ML. et al. Anvi’o: an advanced analysis and visualization platform for ‘omics data. PeerJ. 2015;3:e1319PubMed
PubMed Central
Google Scholar
Nguyen LT, Schmidt HA, von Haeseler A, Minh BQ. IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol Biol Evol. 2015;32:268–74.CAS
Google Scholar
Manefield M, Whiteley AS, Ostle N, Ineson P, Bailey MJ. Technical considerations for RNA- based stable isotope probing an approach to associating microbial diversity with microbial community function. Rapid Commun Mass Spectrom. 2002;16:2179–83.CAS
PubMed
Google Scholar
Lazar CS, Baker BJ, Seitz KW, Teske AP. Genomic reconstruction of multiple lineages of uncultured benthic archaea suggests distinct biogeochemical roles and ecological niches. ISME J. 2017;11:1118–29.CAS
PubMed
PubMed Central
Google Scholar
Villanueva L, Damste JS, Schouten S. A re-evaluation of the archaeal membrane lipid biosynthetic pathway. Nat Rev Microbiol. 2014;12:438–48.CAS
PubMed
Google Scholar
Konstantinidis KT, Rossello-Mora R, Amann R. Uncultivated microbes in need of their own taxonomy. ISME J. 2017;11:2399–406.PubMed
PubMed Central
Google Scholar
Hedges JI, Keil RG. Sedimentary organic matter preservation: an assessment and speculative synthesis. Mar Chem. 1995;49:81–115.CAS
Google Scholar
Arndt S, Jørgensen BB, LaRowe DE, Middelburg JJ, Pancost RD, Regnier P. Quantifying the degradation of organic matter in marine sediments: a review and synthesis. Earth-Sci Rev. 2013;123:53–86.CAS
Google Scholar
LaRowe DE, Arndt S, Bradley JA, Estes ER, Hoarfrost A, Lang SQ, et al. The fate of organic carbon in marine sediments – New insights from recent data and analysis. Earth-Sci Rev. 2020;204:103146.CAS
Google Scholar
Zhu Q-Z, Elvert M, Meador TB, Becker KW, Heuer VB, Hinrichs KU. Stable carbon isotopic compositions of archaeal lipids constrain terrestrial, planktonic, and benthic sources in marine sediments. Geochim Cosmochim Acta. 2021;307:319–37.CAS
Google Scholar
Jain S, Caforio A, Driessen AJ. Biosynthesis of archaeal membrane ether lipids. Front Microbiol. 2014;5:641.PubMed
PubMed Central
Google Scholar
Yang S, Lv Y, Liu X, Wang Y, Fan Q, Yang Z, et al. Genomic and enzymatic evidence of acetogenesis by anaerobic methanotrophic archaea. Nat Commun. 2020;11:3941.CAS
PubMed
PubMed Central
Google Scholar
Zinke LA, Evans PN, Santos-Medellín C, Schroeder AL, Parks DH, Varner RK, et al. Evidence for non-methanogenic metabolisms in globally distributed archaeal clades basal to the Methanomassiliicoccales. Environ Microbiol. 2021;23:340–57.CAS
PubMed
Google Scholar
Bhatnagar L, Jain MK, Aubert JP, Zeikus JG. Comparison of assimilatory organic nitrogen, sulfur, and carbon sources for growth of methanobacterium species. Appl Environ Microbiol. 1984;48:785–90.CAS
PubMed
PubMed Central
Google Scholar
Maupin-Furlow JA. Proteolytic systems of archaea: slicing, dicing, and mincing in the extreme. Emerg Top Life Sci. 2018;2:561–80.CAS
PubMed
PubMed Central
Google Scholar
Pohlschroder M, Pfeiffer F, Schulze S, Abdul Halim MF. Archaeal cell surface biogenesis. FEMS Microbiol Rev. 2018;42:694–717.CAS
PubMed
PubMed Central
Google Scholar
Yancey P, Clark M, Hand S, Bowlus R, Somero G. Living with water stress: evolution of osmolyte systems. Science. 1982;217:1214–22.CAS
PubMed
Google Scholar
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
Oni OE, Schmidt F, Miyatake T, Kasten S, Witt M, Hinrichs KU, et al. Microbial communities and organic matter composition in surface and subsurface sediments of the Helgoland Mud Area, North Sea. Front Microbiol. 2015;6:1290.PubMed
PubMed Central
Google Scholar
Pelikan C, Wasmund K, Glombitza C, Hausmann B, Herbold CW, Flieder M, et al. Anaerobic bacterial degradation of protein and lipid macromolecules in subarctic marine sediment. ISME J. 2021;15:833–47.CAS
PubMed
Google Scholar
Orsi WD, Schink B, Buckel W, Martin WF. Physiological limits to life in anoxic subseafloor sediment. FEMS Microbiol Rev. 2020;44:219–31.CAS
PubMed
PubMed Central
Google Scholar
Heijnen JJ, Van, Dijken JP. In search of a thermodynamic description of biomass yields for the chemotrophic growth of microorganisms. Biotechnol Bioeng. 1992;39:833–58.CAS
PubMed
Google Scholar
Braun S, Mhatre SS, Jaussi M, Røy H, Kjeldsen KU, Pearce C, et al. Microbial turnover times in the deep seabed studied by amino acid racemization modelling. Sci Rep. 2017;7:5680.PubMed
PubMed Central
Google Scholar More