Diversification of methanogens into hyperalkaline serpentinizing environments through adaptations to minimize oxidant limitation

Boyd ES, Amenabar MJ, Poudel S, Templeton AS. Bioenergetic constraints on the origin of autotrophic metabolism. Philos Trans R Soc A. 2020;378:1471–2962.

Article  CAS  Google Scholar 

Boyd ES, Schut GJ, Adams MWW, Peters JW. Hydrogen metabolism and the evolution of biological respiration. Microbe. 2014;9:361–7.

Google Scholar 

Hoehler TM. Biogeochemistry of dihydrogen (H₂). In: Sigel H, and Sigel R (eds.). Metal ions in biological systems. Vol 43. (Taylor & Francis Group, Boca Raton, FL, 2005) pp 9-48.

Weiss MC, Sousa FL, Mrnjavac N, Neukirchen S, Roettger M, Nelson-Sathi S, et al. The physiology and habitat of the last universal common ancestor. Nat Microbiol. 2016;1:1–8.

Google Scholar 

McCollom TM, Klein F, Robbins M, Moskowitz B, Berquó TS, Jöns N, et al. Temperature trends for reaction rates, hydrogen generation, and partitioning of iron during experimental serpentinization of olivine. Geochim Cosmochim Acta. 2016;181:175–200.

CAS  Article  Google Scholar 

Schulte M, Blake D, Hoehler T, McCollom T. Serpentinization and its implications for life on the early Earth and Mars. Astrobiology. 2006;6:364–76.

CAS  PubMed  Article  Google Scholar 

Russell M, Hall A, Martin W. Serpentinization as a source of energy at the origin of life. Geobiology. 2010;8:355–71.

CAS  PubMed  Article  Google Scholar 

Seewald JS, Zolotov MY, McCollom T. Experimental investigation of single carbon compounds under hydrothermal conditions. Geochim Cosmochim Acta. 2006;70:446–60.

CAS  Article  Google Scholar 

McCollom TM, Seewald JS. Abiotic synthesis of organic compounds in deep-sea hydrothermal environments. Chem Rev. 2007;107:382–401.

CAS  PubMed  Article  Google Scholar 

Twing KI, Brazelton WJ, Kubo MDY, Hyer AJ, Cardace D, Hoehler TM, et al. Serpentinization-influenced groundwater harbors extremely low diversity microbial communities adapted to high pH. Front Microbiol. 2017;8:308.

PubMed  PubMed Central  Article  Google Scholar 

Brazelton WJ, Nelson B, Schrenk MO. Metagenomic evidence for H₂ oxidation and H₂ production by serpentinite-hosted subsurface microbial communities. Front Microbiol. 2012;2:268.

PubMed  PubMed Central  Article  Google Scholar 

Morrill PL, Brazelton WJ, Kohl L, Rietze A, Miles SM, Kavanagh H, et al. Investigations of potential microbial methanogenic and carbon monoxide utilization pathways in ultra-basic reducing springs associated with present-day continental serpentinization: the Tablelands, NL, CAN. Front Microbiol. 2014;5:613.

PubMed  PubMed Central  Article  Google Scholar 

Crespo-Medina M, Twing KI, Sánchez-Murillo R, Brazelton WJ, McCollom TM, Schrenk MO. Methane dynamics in a tropical serpentinizing environment: the Santa Elena Ophiolite, Costa Rica. Front Microbiol. 2017;8:916.

PubMed  PubMed Central  Article  Google Scholar 

Woycheese KM, Meyer-Dombard DR, Cardace D, Argayosa AM, Arcilla CA. Out of the dark: transitional subsurface-to-surface microbial diversity in a terrestrial serpentinizing seep (Manleluag, Pangasinan, the Philippines). Front Microbiol. 2015;6:44.

PubMed  PubMed Central  Article  Google Scholar 

Neubeck A, Sun L, Müller B, Ivarsson M, Hosgörmez H, Özcan D, et al. Microbial community structure in a serpentine-hosted abiotic gas seepage at the Chimaera Ophiolite, Turkey. Appl Environ Microbiol. 2017;83:e03430–16.

PubMed  PubMed Central  Article  Google Scholar 

Lang SQ, Früh-Green G, Bernasconi SM, Brazelton WJ, Schrenk MO, McGonigle JM. Deeply-sourced formate fuels sulfate reducers but not methanogens at Lost City hydrothermal field. Sci Rep. 2018;8:1–10.

Article  CAS  Google Scholar 

Brazelton WJ, Morrill PL, Szponar N, Schrenk MO. Bacterial communities associated with subsurface geochemical processes in continental serpentinite springs. Appl Environ Microbiol. 2013;79:3906–16.

CAS  PubMed  PubMed Central  Article  Google Scholar 

Fones EM, Colman DR, Kraus EA, Nothaft DB, Poudel S, Rempfert KR, et al. Physiological adaptations to serpentinization in the Samail Ophiolite, Oman. ISME J. 2019;13:1750–62.

CAS  PubMed  PubMed Central  Article  Google Scholar 

Rempfert KR, Miller HM, Bompard N, Nothaft D, Matter JM, Kelemen P, et al. Geological and geochemical controls on subsurface microbial life in the Samail Ophiolite, Oman. Front Microbiol. 2017;8:56.

PubMed  PubMed Central  Article  Google Scholar 

Kelemen PB, Matter J, Streit EE, Rudge JF, Curry WB, Blusztajn J. Rates and mechanisms of mineral carbonation in peridotite: natural processes and recipes for enhanced, in situ CO₂ capture and storage. Annu Rev Earth Planet Sci. 2011;39:545–76.

CAS  Article  Google Scholar 

Canovas PA, Hoehler T, Shock EL. Geochemical bioenergetics during low-temperature serpentinization: an example from the Samail ophiolite, Sultanate of Oman. J Geophys Res. 2017;122:1821–47.

Article  Google Scholar 

Suzuki S, Ishii S, Wu A, Cheung A, Tenney A, Wanger G, et al. Microbial diversity in The Cedars, an ultrabasic, ultrareducing, and low salinity serpentinizing ecosystem. Proc Natl Acad Sci USA. 2013;110:15336–41.

CAS  PubMed  Article  Google Scholar 

Brazelton WJ, Thornton CN, Hyer A, Twing KI, Longino AA, Lang SQ, et al. Metagenomic identification of active methanogens and methanotrophs in serpentinite springs of the Voltri Massif, Italy. Peer J. 2017;5:e2945.

PubMed  Article  CAS  Google Scholar 

Morrill PL, Kuenen JG, Johnson OJ, Suzuki S, Rietze A, Sessions AL, et al. Geochemistry and geobiology of a present-day serpentinization site in California: The Cedars. Geochim Cosmochim Acta. 2013;109:222–40.

CAS  Article  Google Scholar 

Miller HM, Matter JM, Kelemen P, Ellison ET, Conrad ME, Fierer N, et al. Modern water/rock reactions in Oman hyperalkaline peridotite aquifers and implications for microbial habitability. Geochim Cosmochim Acta. 2016;179:217–41.

CAS  Article  Google Scholar 

Russell MJ, Martin W. The rocky roots of the acetyl-CoA pathway. Trends Biochem Sci. 2004;29:358–63.

CAS  PubMed  Article  Google Scholar 

Martin WF, Weiss MC, Neukirchen S, Nelson-Sathi S, Sousa FL. Physiology, phylogeny, and LUCA. Microbial. Cell. 2016;3:582–7.

Google Scholar 

Ueno Y, Yamada K, Yoshida N, Maruyama S, Isozake Y. Evidence from fluid inclusions for microbial methanogenesis in the early Archaean era. Nature. 2006;440:516–9.

CAS  PubMed  Article  Google Scholar 

Moore EK, Jelen BI, Giovannelli D, Raanan H, Falkowski PG. Metal availability and the expanding network of microbial metabolisms in the Archaean eon. Nat Geosci. 2017;10:629–36.

CAS  Article  Google Scholar 

Etiope G, Vadillo I, Whiticar MJ, Marques JM, Carreira PM, Tiago I, et al. Abiotic methane seepage in the Ronda peridotite massif, southern Spain. Appl Geochem. 2016;66:101–13.

CAS  Google Scholar 

Proskurowski G, Lilley MD, Seewald JS, Früh-Green G, Olson EJ, Lupton JE, et al. Abiogenic hydrocarbon production at Lost City hydrothermal field. Science. 2008;319:604–7.

CAS  PubMed  Article  Google Scholar 

Etiope G. Methane origin in the Samail ophiolite: Comment on “Modern water/rock reactions in Oman hyperalkaline peridotite aquifers and implications for microbial habitability”. Geochim Cosmochim Acta. 2017;197:467–70.

CAS  Article  Google Scholar 

Miller HM, Matter JM, Kelemen P, Ellison ET, Conrad ME, Fierer N, et al. Reply to “Methane origin in the Samail ophiolite: Comment on ‘Modern water/rock reactions in Oman hyperalkaline peridotite aquifers and implications for microbial habitability’”. Geochim Cosmochim Acta. 2017;197:471–3.

CAS  Article  Google Scholar 

Miller HM, Chaudhry N, Conrad ME, Markus B, Kopf SH, Templeton AS. Large carbon isotope variability during methanogenesis under alkaline conditions. Geochim Cosmochim Acta. 2018;237:18–31.

CAS  Article  Google Scholar 

Bradley AS, Hayes JM, Summons RE. Extraordinary ¹³C enrichment of diether lipids at the Lost City Hydrothermal Field indicates a carbon-limited ecosystem. Geochim Cosmochim Acta. 2009;73:102–18.

CAS  Article  Google Scholar 

Zwicker J, Birgel D, Bach W, Richoz S, Smrzka D, Grasemann B, et al. Evidence for archaeal methanogenesis within veins at the onshore serpentinite-hosted Chimaera seeps, Turkey. Chem Geol. 2018;483:567–80.

CAS  Article  Google Scholar 

Kraus EA, Stamps BW, Rempfert KR, Nothaft DB, Boyd ES, Matter JM, et al. Biological methane cycling in serpentinization-impacted fluids of the Samail ophiolite of Oman. AGU Fall Meeting Abstracts. 2018; (abstract #V13E-0139).

Miller HM, Mayhew LE, Ellison ET, Kelemen P, Kubo M, Templeton AS. Low temperature hydrogen production during experimental hydration of partially-serpentinized dunite. Geochim Cosmochim Acta. 2017;209:161–83.

CAS  Article  Google Scholar 

Neal C, Stanger G. Hydrogen generation from mantle source rocks in Oman. Earth Planet Sci Lett. 1983;66:315–20.

CAS  Article  Google Scholar 

Streit E, Kelemen P, Eiler J. Coexisting serpentine and quartz from carbonate-bearing serpentinized peridotite in the Samail Ophiolite, Oman. Contrib Miner Petr. 2012;164:821–37.

CAS  Article  Google Scholar 

Chavagnac V, Monnin C, Ceuleneer G, Boulart C, Hoareau G. Characterization of hyperalkaline fluids produced by low-temperature serpentinization of mantle peridotites in the Oman and Ligurian ophiolites. Geochem Geophys. 2013;14:2496–522.

CAS  Article  Google Scholar 

Mervine EM, Humphris SE, Sims KWW, Kelemen PB, Jenkins WJ. Carbonation rates of peridotite in the Samail Ophiolite, Sultanate of Oman, constrained through ¹⁴C dating and stable isotopes. Geochim Cosmochim Acta. 2014;126:371–97.

CAS  Article  Google Scholar 

Kang DWD, Froula J, Egan R, Wang Z. MetaBAT, an efficient tool for accurately reconstructing single genomes from complex microbial communities. PeerJ. 2015;3:e1165.

PubMed  PubMed Central  Article  CAS  Google Scholar 

Stepanauskas R, Fergusson EA, Brown J, Poulton NJ, Tupper B, Labonté JM, et al. Improved genome recovery and integrated cell-size analyses of individual uncultured microbial cells and viral particles. Nat Commun. 2017;8:84.

PubMed  PubMed Central  Article  CAS  Google Scholar 

Colman DR, Lindsay MR, Boyd ES. Mixing of meteoric and geothermal fluids supports hyperdiverse chemosynthetic hydrothermal communities. Nat Commun. 2019;10:1–13.

Article  CAS  Google Scholar 

Wu M, Scott AJ. Phylogenomic analysis of bacterial and archaeal sequences with AMPHORA2. J Bioinform. 2012;28:1033–4.

CAS  Article  Google Scholar 

Sievers F, Wilm A, Dineen D, Gibson TJ, Karplus K, Li W, et al. Fast, scalable generation of highquality protein multiple sequence alignments using Clustal Omega. Mol Syst Biol. 2011;7:539.

PubMed  PubMed Central  Article  Google Scholar 

Nguyen LT, Schmidt HA, von Haesler A, Minh BQ. IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol Biol Evol. 2015;32:268–74.

CAS  PubMed  PubMed Central  Article  Google Scholar 

Kalyaanamoorthy S, Minh BQ, Wong TKF, von Haesler A, Jermiin LS. ModelFinder: fast model selection for accurate phylogenetic estimates. Nat Methods. 2017;14:587.

CAS  PubMed  PubMed Central  Article  Google Scholar 

Hyatt D, Chen GL, LoCascio PF, Land ML, Larimer FW, Hauser LJ. Prodigal: prokaryotic gene recognition and translation initiation site identification. BMC Bioinform. 2010;11:119.

Article  CAS  Google Scholar 

Seemann T. Prokka: rapid prokaryotic genome annotation. J Bioinform. 2014;30:2068–9.

CAS  Article  Google Scholar 

Kanehisa M, Goto S. KEGG: Kyoto encyclopedia of genes and genomes. Nucleic Acids Res. 2000;28:27–30.

CAS  PubMed  PubMed Central  Article  Google Scholar 

Moriya Y, Itoh M, Okuda S, Yoshizawa AC, Kanehisa M. KAAS: an automatic genome annotation and pathway reconstruction server. Nucleic Acids Res. 2007;35:W182–5.

PubMed  PubMed Central  Article  Google Scholar 

Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol. 1990;215:403–10.

CAS  PubMed  PubMed Central  Article  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  Article  Google Scholar 

Greening C, Biswas A, Carere CR, Jackson CJ, Taylor MC, Stott MB, et al. Genomic and metagenomic surveys of hydrogenase distribution indicate H₂ is a widely utilised energy source for microbial growth and survival. ISME J. 2016;10:761–77.

CAS  PubMed  Article  Google Scholar 

Peters JW, Schut GJ, Boyd ES, Mulder DW, Shepard EM, Broderick JB, et al. [FeFe]-and [NiFe]-hydrogenase diversity, mechanism, and maturation. BBA-Mol Cell Res. 2015;1853:1350–69.

CAS  Google Scholar 

Marchler-Bauer A, Bo Y, Han L, He J, Lanczycki CJ, Lu S, et al. CDD/SPARCLE: functional classification of proteins via subfamily domain architectures. Nucleic Acids Res. 2016;45:D200–3.

PubMed  PubMed Central  Article  CAS  Google Scholar 

Marçais G, Delcher AL, Phillippy AM, Coston R, Salzberg SL, Zimin A. MUMmer4: a fast and versatile genome alignment system. PLoS Comput Biol. 2018;14:e1005944.

PubMed  PubMed Central  Article  CAS  Google Scholar 

R Core Team, R: a language and environment for statistical computing. Version 3.0.1. R Foundation for Statistical Computing. 2013.

Leplae R, Lima-Mendez G, Toussaint A. ACLAME: a CLAssification of Mobile genetic Elements, update 2010. Nucleic Acids Res. 2010;38:D57–D61.

CAS  PubMed  Article  Google Scholar 

Lefort V, Longueville J-E, Gascuel O. SMS: smart model selection in PhyML. Mol Biol Evol. 2017;34:2422–4.

CAS  PubMed  PubMed Central  Article  Google Scholar 

Guindon S, Dufayard J-F, Lefort V, Anisimova M, Hordijk W, Gascuel O. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol. 2010;59:307–21.

CAS  PubMed  Article  Google Scholar 

Darling AE, Mau B, Perna NT. progressiveMauve: multiple genome alignment with gene gain, loss and rearrangement. PloS One. 2010;5:e11147.

PubMed  PubMed Central  Article  CAS  Google Scholar 

Harrison KJ, Crécy-Lagard V, Zallot R. Gene Graphics: a genomic neighborhood data visualization web application. J Bioinform. 2018;34:1406–8.

CAS  Article  Google Scholar 

Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, and O’Hara RB vegan: community ecology package. R Foundation for Statistical Computing. 2015.

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;25:725–31.

Article  CAS  Google Scholar 

Suzuki S, Ishii S, Hoshino T, Rietze A, Tenney A, Morrill PL, et al. Unusual metabolic diversity of hyperalkaliphilic microbial communities associated with subterranean serpentinization at The Cedars. ISME J. 2017;11:2584–98.

PubMed  PubMed Central  Article  Google Scholar 

Giovannoni SJ, Thrash JC, Temperton B. Implications of streamlining theory for microbial ecology. ISME J. 2014;8:1553–65.

PubMed  PubMed Central  Article  Google Scholar 

Thauer RK, Kaster AK, Seedorf H, Buckel W, Hedderich R. Methanogenic archaea: ecologically relevant differences in energy conservation. Nat Rev Microbiol. 2008;6:579–91.

CAS  PubMed  Article  Google Scholar 

Hendrickson EL, Leigh JA. Roles of coenzyme F₄₂₀-reducing hydrogenases and hydrogen-and F₄₂₀-dependent methylenetetrahydromethanopterin dehydrogenases in reduction of F₄₂₀ and production of hydrogen during methanogenesis. J Bacteriol. 2008;190:4818–21.

CAS  PubMed  PubMed Central  Article  Google Scholar 

Goldman AD, Leigh JA, Samudrala R. Comprehensive computational analysis of Hmd enzymes and paralogs in methanogenic Archaea. BMC Evol Biol. 2009;9:199.

PubMed  PubMed Central  Article  CAS  Google Scholar 

Tersteegen A, Hedderich R. Methanobacterium thermoautotrophicum encodes two multisubunit membrane‐bound [NiFe] hydrogenases: transcription of the operons and sequence analysis of the deduced proteins. Eur J Biochem. 1999;264:930–43.

CAS  PubMed  Article  Google Scholar 

Lie TJ, Costa KC, Lupa B, Korpole S, Whitman WB, Leigh JA. Essential anaplerotic role for the energy-converting hydrogenase Eha in hydrogenotrophic methanogenesis. Proc Natl Acad Sci USA. 2012;109:15473–8.

CAS  PubMed  Article  Google Scholar 

Thauer RK. The Wolfe cycle comes full circle. Proc Natl Acad Sci USA. 2012;109:15084–5.

CAS  PubMed  Article  Google Scholar 

Costa KC, Wong PM, Wang T, Lie TJ, Dodsworth JA, Swanson I, et al. Protein complexing in a methanogen suggests electron bifurcation and electron delivery from formate to heterodisulfide reductase. Proc Natl Acad Sci USA. 2010;107:11050–5.

CAS  PubMed  Article  Google Scholar 

Greening C, Ahmed FA, Mohamed AE, Lee BM, Pandey G, Warden AC, et al. Physiology, biochemistry, and applications of F420-and Fo-dependent redox reactions. Microbiol Mol Biol Rev. 2016;80:451–93.

CAS  PubMed  PubMed Central  Article  Google Scholar 

Yan Z, Ferry JG. Electron bifurcation and confurcation in methanogenesis and reverse methanogenesis. Front Microbiol. 2018;9:1322.

PubMed  PubMed Central  Article  Google Scholar 

Costa KC, Lie TJ, Xia Q, Leigh JA. VhuD facilitates electron flow from H₂ or formate to heterodisulfide reductase in Methanococcus maripaludis. J Bacteriol. 2013;195:5160–5.

CAS  PubMed  PubMed Central  Article  Google Scholar 

Schauer NL, Ferry JG. Properties of formate dehydrogenase in Methanobacterium formicicum. J Bacteriol. 1982;150:1–7.

CAS  PubMed  PubMed Central  Article  Google Scholar 

Schauer NL, Ferry JG, Honek JF, Orme-Johnson WH, Walsh C. Mechanistic studies of the coenzyme F420-reducing formate dehydrogenase from Methanobacterium formicicum. Biochemistry. 1986;25:7163–8.

CAS  PubMed  Article  Google Scholar 

Mills DJ, Vitt S, Strauss M, Shima S, Vonck J. De novo modeling of the F₄₂₀-reducing [NiFe]-hydrogenase from a methanogenic archaeon by cryo-electron microscopy. Elife. 2013;2:e00218.

PubMed  PubMed Central  Article  Google Scholar 

Schut GJ, Boyd ES, Peters JW, Adams MWW. The modular respiratory complexes involved in hydrogen and sulfur metabolism by heterotrophic hyperthermophilic archaea and their evolutionary implications. FEMS Microbiol Rev. 2013;37:182–203.

CAS  PubMed  Article  Google Scholar 

Hamamoto T, Hashimoto M, Hino M, Kitada M, Seto Y, Kudo T, et al. Characterization of a gene responsible for the Na⁺/H⁺ antiporter system of alkalophilic Bacillus species strain C125. Mol Microbiol. 1994;14:939–46.

CAS  PubMed  Article  Google Scholar 

Buckel W, Thauer RK. Energy conservation via electron bifurcating ferredoxin reduction and proton/Na⁺ translocating ferredoxin oxidation. BBA-Bioenerg. 2013;1827:94–113.

CAS  Article  Google Scholar 

Boone DR, Johnson RL, Liu Y. Diffusion of the interspecies electron carriers H₂ and formate in methanogenic ecosystems and its implications in the measurement of K_m for H₂ or formate uptake. Appl Environ Microbiol. 1989;55:1735–41.

CAS  PubMed  PubMed Central  Article  Google Scholar 

Suzuki S, Nealson KH, Ishii S. Genomic and in-situ transcriptomic characterization of the candidate phylum NPL-UPL2 from highly alkaline highly reducing serpentinized groundwater. Front Micrbiol. 2018;9:3141.

Article  Google Scholar 

Lang SQ, Butterfield DA, Schulte M, Kelley DS, Lilley MD. Elevated concentrations of formate, acetate and dissolved organic carbon found at the Lost City hydrothermal field. Geochim Cosmochim Acta. 2010;74:941–52.

CAS  Article  Google Scholar 

McCollom TM, Seewald JS. Experimental constraints on the hydrothermal reactivity of organic acids and acid anions: I. Formic acid and formate. Geochim Cosmochim Acta. 2003;67:3625–44.  

CAS  Article  Google Scholar 

Zeng Y, Liu J. Short-chain carboxylates in fluid inclusions in minerals. Appl Geochem. 2000;15:13–25.

CAS  Article  Google Scholar 

Brazelton WJ, Baross JA. Abundant transposases encoded by the metagenome of a hydrothermal chimney biofilm. ISME J. 2009;3:1420–4.

CAS  PubMed  Article  Google Scholar 

Zhang J, Kasciukovic T, White MF. The CRISPR associated protein Cas4 Is a 5′ to 3′ DNA exonuclease with an iron-sulfur cluster. PloS One. 2012;7:e47232.

CAS  PubMed  PubMed Central  Article  Google Scholar 

Rath D, Amlinger L, Rath A, Lundgren M. The CRISPR-Cas immune system: biology, mechanisms and applications. Biochimie. 2015;117:119–28.

CAS  PubMed  Article  Google Scholar 

Jansen R, van Embden JDA, Gaastra W, Schouls LM. Identification of genes that are associated with DNA repeats in prokaryotes. Mol Microbiol. 2002;43:1565–75.

CAS  PubMed  PubMed Central  Article  Google Scholar 

Reno ML, Held NL, Fields CJ, Burke PV, Whitaker RJ. Biogeography of the Sulfolobus islandicus pan-genome. Proc Natl Acad Sci USA. 2009;106:8605–10.

CAS  PubMed  Article  Google Scholar 

Tettelin H, Masignani V, Cieslewicz MJ, Donati C, Medini D, Ward NL, et al. Genome analysis of multiple pathogenic isolates of Streptococcus agalactiae: implications for the microbial “pan-genome.”. Proc Natl Acad Sci USA. 2005;102:13950–5.

CAS  PubMed  Article  Google Scholar 

Labonté JM, Field EK, Lau M, Chivian D, Van Heerden E, Wommack KE, et al. Single cell genomics indicates horizontal gene transfer and viral infections in a deep subsurface Firmicutes population. Front Microbiol. 2015;6:349.

PubMed  PubMed Central  Google Scholar 

Karnachuk OV, Frank YA, Lukina AP, Kadnikov VV, Beletsky AV, Mardanov AV, et al. Domestication of previously uncultivated Candidatus Desulforudis audaxviator from a deep aquifer in Siberia sheds light on its physiology and evolution. ISME J. 2019;13:1947–59.

CAS  PubMed  PubMed Central  Article  Google Scholar 

Paul BG, Burstein D, Castelle CJ, Handa S, Arambula D, Czornyj E, et al. Retroelement-guided protein diversificiation abounds in vast lineages of bacteria and archaea. Nat Microbiol. 2017;2:17045.

CAS  PubMed  PubMed Central  Article  Google Scholar 

Dirix G, Monsieurs P, Dombrecht B, Daniels R, Marchal K, Vanderleyden J, et al. Peptide signal molecules and bacteriocins in Gram-negative bacteria: a genome-wide in silico screening for peptides containing a double-glycine leader sequence and their cognate transporters. Peptides. 2004;25:1425–40.

CAS  PubMed  Article  Google Scholar