CoChat
Sign Up
Cited by 57Methane Hydrates and Related PhenomenaMicrobial metabolism and enzyme functionMicrobial Community Ecology and Physiology

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

Open access
Fones, Elizabeth M, Colman, Daniel R, Kraus, Emily A, Stepanauskas, Ramunas, Templeton, Alexis S, Spear, John R, Boyd, Eric S·2021·The ISME Journal
DOI 10.1038/s41396-020-00838-1PMC PMC8115248
Open this paper in CoChat — free account

Abstract

Metagenome assembled genomes (MAGs) and single amplified genomes (SAGs) affiliated with two distinct Methanobacterium lineages were recovered from subsurface fracture waters of the Samail Ophiolite, Sultanate of Oman. Lineage Type I was abundant in waters with circumneutral pH, whereas lineage Type II was abundant in hydrogen rich, hyperalkaline waters. Type I encoded proteins to couple hydrogen oxidation to CO2 reduction, typical of hydrogenotrophic methanogens. Surprisingly, Type II, which branched from the Type I lineage, lacked homologs of two key oxidative [NiFe]-hydrogenases. These functions were presumably replaced by formate dehydrogenases that oxidize formate to yield reductant and cytoplasmic CO2 via a pathway that was unique among characterized Methanobacteria, allowing cells to overcome CO2/oxidant limitation in high pH waters. This prediction was supported by microcosm-based radiotracer experiments that showed significant biological methane generation from formate, but not bicarbonate, in waters where the Type II lineage was detected in highest relative abundance. Phylogenetic analyses and variability in gene content suggested that recent and ongoing diversification of the Type II lineage was enabled by gene transfer, loss, and transposition. These data indicate that selection imposed by CO2/oxidant availability drove recent methanogen diversification into hyperalkaline waters that are heavily impacted by serpentinization.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1038/s41396-020-00838-1

Cites

15 of 15 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Cites

Flagged first, then by citations

Research works printed but not linked: 81

  1. [3]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. 16370113
  2. [5]McCollom TM Klein F Robbins M Moskowitz B Berquó TS Jöns N Temperature trends for reaction rates, hydrogen generation, and partitioning of iron during experimental serpentinization of olivine Geochim Cosmochim Acta 2016 181 175 200 10.1016/j.gca.2016.03.002 · DOI
  3. [7]Russell M Hall A Martin W Serpentinization as a source of energy at the origin of life Geobiology 2010 8 355 71 10.1111/j.1472-4669.2010.00249.x 20572872 · DOI · Paper page
  4. [8]Seewald JS Zolotov MY McCollom T Experimental investigation of single carbon compounds under hydrothermal conditions Geochim Cosmochim Acta 2006 70 446 60 10.1016/j.gca.2005.09.002 · DOI
  5. [9]McCollom TM Seewald JS Abiotic synthesis of organic compounds in deep-sea hydrothermal environments Chem Rev 2007 107 382 401 10.1021/cr0503660 17253758 · DOI
  6. [10]Twing KI Brazelton WJ Kubo MDY Hyer AJ Cardace D Hoehler TM Serpentinization-influenced groundwater harbors extremely low diversity microbial communities adapted to high pH Front Microbiol 2017 8 308 10.3389/fmicb.2017.00308 28298908 PMC5331062 · DOI
  7. [11]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 10.3389/fmicb.2011.00268 22232619 PMC3252642 · DOI
  8. [12]Morrill PL Brazelton WJ Kohl L Rietze A Miles SM Kavanagh H 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 10.3389/fmicb.2014.00613 25431571 PMC4230201 · DOI
  9. [13]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 10.3389/fmicb.2017.00916 28588569 PMC5440473 · DOI
  10. [14]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 10.3389/fmicb.2015.00044 25745416 PMC4333863 · DOI
  11. [15]Neubeck A Sun L Müller B Ivarsson M Hosgörmez H Özcan D Microbial community structure in a serpentine-hosted abiotic gas seepage at the Chimaera Ophiolite, Turkey Appl Environ Microbiol 2017 83 e03430 16 10.1128/AEM.03430-16 28389534 PMC5452829 · DOI
  12. [16]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 29335466 PMC5768773
  13. [17]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 10.1128/AEM.00330-13 23584766 PMC3697581 · DOI
  14. [18]Fones EM Colman DR Kraus EA Nothaft DB Poudel S Rempfert KR Physiological adaptations to serpentinization in the Samail Ophiolite, Oman ISME J 2019 13 1750 62 10.1038/s41396-019-0391-2 30872803 PMC6588467 · DOI
  15. [20]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 10.1146/annurev-earth-092010-152509 · DOI · Paper page
  16. [21]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 10.1002/2017JG003825 · DOI
  17. [22]Suzuki S Ishii S Wu A Cheung A Tenney A Wanger G Microbial diversity in The Cedars, an ultrabasic, ultrareducing, and low salinity serpentinizing ecosystem Proc Natl Acad Sci USA 2013 110 15336 41 10.1073/pnas.1302426110 24003156 PMC3780913 · DOI · Paper page
  18. [23]Brazelton WJ Thornton CN Hyer A Twing KI Longino AA Lang SQ Metagenomic identification of active methanogens and methanotrophs in serpentinite springs of the Voltri Massif, Italy Peer J 2017 5 e2945 10.7717/peerj.2945 28149702 PMC5274519 · DOI
  19. [24]Morrill PL Kuenen JG Johnson OJ Suzuki S Rietze A Sessions AL Geochemistry and geobiology of a present-day serpentinization site in California: The Cedars Geochim Cosmochim Acta 2013 109 222 40 10.1016/j.gca.2013.01.043 · DOI · Paper page
  20. [25]Miller HM Matter JM Kelemen P Ellison ET Conrad ME Fierer N Modern water/rock reactions in Oman hyperalkaline peridotite aquifers and implications for microbial habitability Geochim Cosmochim Acta 2016 179 217 41 10.1016/j.gca.2016.01.033 · DOI
  21. [26]Russell MJ Martin W The rocky roots of the acetyl-CoA pathway Trends Biochem Sci 2004 29 358 63 10.1016/j.tibs.2004.05.007 15236743 · DOI · Paper page
  22. [27]Martin WF Weiss MC Neukirchen S Nelson-Sathi S Sousa FL Physiology, phylogeny, and LUCA. Microbial Cell 2016 3 582 7 PMC5348977 28357330
  23. [29]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 10.1038/ngeo3006 · DOI
  24. [32]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 10.1016/j.gca.2016.08.001 · DOI
  25. [33]Miller HM Matter JM Kelemen P Ellison ET Conrad ME Fierer N 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 10.1016/j.gca.2016.11.011 · DOI
  26. [34]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 10.1016/j.gca.2018.06.007 · DOI · Paper page
  27. [35]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 10.1016/j.gca.2008.10.005 · DOI
  28. [36]Zwicker J Birgel D Bach W Richoz S Smrzka D Grasemann B Evidence for archaeal methanogenesis within veins at the onshore serpentinite-hosted Chimaera seeps, Turkey Chem Geol 2018 483 567 80 10.1016/j.chemgeo.2018.03.027 · DOI
  29. [38]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 10.1016/j.gca.2017.04.022 · DOI
  30. [39]Neal C Stanger G Hydrogen generation from mantle source rocks in Oman Earth Planet Sci Lett 1983 66 315 20 10.1016/0012-821X(83)90144-9 · DOI
  31. [40]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 10.1007/s00410-012-0775-z · DOI · Paper page
  32. [41]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 10.1002/ggge.20147 · DOI · Paper page
  33. [43]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 10.7717/peerj.1165 26336640 PMC4556158 · DOI
  34. [44]Stepanauskas R Fergusson EA Brown J Poulton NJ Tupper B Labonté JM Improved genome recovery and integrated cell-size analyses of individual uncultured microbial cells and viral particles Nat Commun 2017 8 84 10.1038/s41467-017-00128-z 28729688 PMC5519541 · DOI
  35. [45]Colman DR Lindsay MR Boyd ES Mixing of meteoric and geothermal fluids supports hyperdiverse chemosynthetic hydrothermal communities Nat Commun 2019 10 1 13 10.1038/s41467-019-08499-1 30737379 PMC6368606 · DOI
  36. [46]Wu M Scott AJ Phylogenomic analysis of bacterial and archaeal sequences with AMPHORA2 J Bioinform 2012 28 1033 4 10.1093/bioinformatics/bts079 22332237 · DOI
  37. [47]Sievers F Wilm A Dineen D Gibson TJ Karplus K Li W Fast, scalable generation of highquality protein multiple sequence alignments using Clustal Omega Mol Syst Biol 2011 7 539 10.1038/msb.2011.75 21988835 PMC3261699 · DOI
  38. [48]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 10.1093/molbev/msu300 25371430 PMC4271533 · DOI · Paper page
  39. [50]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 10.1186/1471-2105-11-119 PMC2848648 20211023 · DOI
  40. [51]Seemann T Prokka: rapid prokaryotic genome annotation J Bioinform 2014 30 2068 9 10.1093/bioinformatics/btu153 24642063 · DOI
  41. [52]Kanehisa M Goto S KEGG: Kyoto encyclopedia of genes and genomes Nucleic Acids Res 2000 28 27 30 10.1093/nar/28.1.27 10592173 PMC102409 · DOI · Paper page
  42. [53]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 10.1093/nar/gkm321 17526522 PMC1933193 · DOI
  43. [54]Altschul SF Gish W Miller W Myers EW Lipman DJ Basic local alignment search tool J Mol Biol 1990 215 403 10 10.1016/S0022-2836(05)80360-2 2231712 · DOI · Paper page
  44. [55]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 10.1101/gr.186072.114 25977477 PMC4484387 · DOI · Paper page
  45. [56]Greening C Biswas A Carere CR Jackson CJ Taylor MC Stott MB 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 10.1038/ismej.2015.153 26405831 PMC4817680 · DOI
  46. [57]Peters JW Schut GJ Boyd ES Mulder DW Shepard EM Broderick JB [FeFe]-and [NiFe]-hydrogenase diversity, mechanism, and maturation BBA-Mol Cell Res 2015 1853 1350 69 25461840
  47. [58]Marchler-Bauer A Bo Y Han L He J Lanczycki CJ Lu S CDD/SPARCLE: functional classification of proteins via subfamily domain architectures Nucleic Acids Res 2016 45 D200 3 10.1093/nar/gkw1129 27899674 PMC5210587 · DOI
  48. [59]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 10.1371/journal.pcbi.1005944 29373581 PMC5802927 · DOI · Paper page
  49. [61]Leplae R Lima-Mendez G Toussaint A ACLAME: a CLAssification of Mobile genetic Elements, update 2010 Nucleic Acids Res 2010 38 D57 D61 10.1093/nar/gkp938 19933762 PMC2808911 · DOI
  50. [62]Lefort V Longueville J-E Gascuel O SMS: smart model selection in PhyML Mol Biol Evol 2017 34 2422 4 10.1093/molbev/msx149 28472384 PMC5850602 · DOI
  51. [63]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 10.1093/sysbio/syq010 20525638 · DOI · Paper page
  52. [65]Harrison KJ Crécy-Lagard V Zallot R Gene Graphics: a genomic neighborhood data visualization web application J Bioinform 2018 34 1406 8 10.1093/bioinformatics/btx793 PMC5905594 29228171 · DOI
  53. [67]Bowers RM Kyrpides NC Stepanauskas R Harmon-Smith M Doud D Reddy TBK Minimum information about a single amplified genome (MISAG) and a metagenome-assembled genome (MIMAG) of bacteria and archaea Nat Biotechnol 2017 25 725 31 10.1038/nbt.3893 PMC6436528 28787424 · DOI · Paper page
  54. [69]Giovannoni SJ Thrash JC Temperton B Implications of streamlining theory for microbial ecology ISME J 2014 8 1553 65 10.1038/ismej.2014.60 24739623 PMC4817614 · DOI
  55. [70]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 10.1038/nrmicro1931 18587410 · DOI · Paper page
  56. [71]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 10.1128/JB.00255-08 18487331 PMC2447022 · DOI
  57. [72]Goldman AD Leigh JA Samudrala R Comprehensive computational analysis of Hmd enzymes and paralogs in methanogenic Archaea BMC Evol Biol 2009 9 199 10.1186/1471-2148-9-199 19671178 PMC2739858 · DOI
  58. [73]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 10.1046/j.1432-1327.1999.00692.x 10491142 · DOI
  59. [74]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 10.1073/pnas.1208779109 22872868 PMC3458328 · DOI
  60. [75]Thauer RK The Wolfe cycle comes full circle Proc Natl Acad Sci USA 2012 109 15084 5 10.1073/pnas.1213193109 22955879 PMC3458314 · DOI
  61. [77]Greening C Ahmed FA Mohamed AE Lee BM Pandey G Warden AC Physiology, biochemistry, and applications of F420-and Fo-dependent redox reactions Microbiol Mol Biol Rev 2016 80 451 93 10.1128/MMBR.00070-15 27122598 PMC4867364 · DOI
  62. [78]Yan Z Ferry JG Electron bifurcation and confurcation in methanogenesis and reverse methanogenesis Front Microbiol 2018 9 1322 10.3389/fmicb.2018.01322 29973922 PMC6019823 · DOI
  63. [79]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 10.1128/JB.00895-13 24039260 PMC3811579 · DOI
  64. [80]Schauer NL Ferry JG Properties of formate dehydrogenase in Methanobacterium formicicum J Bacteriol 1982 150 1 7 10.1128/jb.150.1.1-7.1982 7061389 PMC220075 · DOI
  65. [81]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 10.1021/bi00370a059 3801411 · DOI
  66. [82]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 10.7554/eLife.00218 23483797 PMC3591093 · DOI
  67. [83]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 10.1111/j.1574-6976.2012.00346.x 22713092 · DOI
  68. [84]Hamamoto T Hashimoto M Hino M Kitada M Seto Y Kudo T Characterization of a gene responsible for the Na+/H+ antiporter system of alkalophilic Bacillus species strain C125 Mol Microbiol 1994 14 939 46 10.1111/j.1365-2958.1994.tb01329.x 7715455 · DOI
  69. [86]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 Km for H2 or formate uptake Appl Environ Microbiol 1989 55 1735 41 10.1128/aem.55.7.1735-1741.1989 16347966 PMC202943 · DOI
  70. [89]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 10.1016/S0016-7037(03)00136-4 · DOI
  71. [90]Zeng Y Liu J Short-chain carboxylates in fluid inclusions in minerals Appl Geochem 2000 15 13 25 10.1016/S0883-2927(99)00020-7 · DOI
  72. [91]Brazelton WJ Baross JA Abundant transposases encoded by the metagenome of a hydrothermal chimney biofilm ISME J 2009 3 1420 4 10.1038/ismej.2009.79 19571895 · DOI
  73. [92]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 10.1371/journal.pone.0047232 23056615 PMC3466216 · DOI
  74. [93]Rath D Amlinger L Rath A Lundgren M The CRISPR-Cas immune system: biology, mechanisms and applications Biochimie 2015 117 119 28 10.1016/j.biochi.2015.03.025 25868999 · DOI
  75. [94]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 10.1046/j.1365-2958.2002.02839.x 11952905 · DOI
  76. [95]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 10.1073/pnas.0808945106 19435847 PMC2689034 · DOI
  77. [96]Tettelin H Masignani V Cieslewicz MJ Donati C Medini D Ward NL Genome analysis of multiple pathogenic isolates of Streptococcus agalactiae: implications for the microbial “pan-genome.” Proc Natl Acad Sci USA 2005 102 13950 5 10.1073/pnas.0506758102 16172379 PMC1216834 · DOI
  78. [97]Labonté JM Field EK Lau M Chivian D Van Heerden E Wommack KE Single cell genomics indicates horizontal gene transfer and viral infections in a deep subsurface Firmicutes population Front Microbiol 2015 6 349 25954269 PMC4406082
  79. [98]Karnachuk OV Frank YA Lukina AP Kadnikov VV Beletsky AV Mardanov AV 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 10.1038/s41396-019-0402-3 30899075 PMC6776058 · DOI
  80. [99]Paul BG Burstein D Castelle CJ Handa S Arambula D Czornyj E Retroelement-guided protein diversificiation abounds in vast lineages of bacteria and archaea Nat Microbiol 2017 2 17045 10.1038/nmicrobiol.2017.45 28368387 PMC5436926 · DOI
  81. [100]Dirix G Monsieurs P Dombrecht B Daniels R Marchal K Vanderleyden J 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 10.1016/j.peptides.2003.10.028 15374646 · DOI

Cited by

Sorted by citations

Authors
Fones, E. M., Colman, D. R., Kraus, E. A., Stepanauskas, R., Templeton, A. S., Spear, J. R., & Boyd, E. S.
Affiliations
  • Montana State University (US)
  • Colorado School of Mines (US)
  • Bigelow Laboratory for Ocean Sciences , East Boothbay, ME 04544, USA
  • University of Colorado Boulder (US)
Corresponding author
Boyd, Eric S
ORCID
Venue
The ISME Journal
Publisher
Oxford University Press (OUP)
Published
2020-11-30
Volume
15
Issue
4
Pages
1121-1135
ISSN
  • 1751-7362 (ISSN-L)
  • 1751-7370
DOI
10.1038/s41396-020-00838-1
PMC
PMC8115248
OpenAlex
W3107208872
Cited by
57
References
15
Citations by year
2026: 9 · 2025: 9 · 2024: 6 · 2023: 11 · 2022: 12 · 2021: 10
FWCI
3.06
Type
journal article
Language
en
Open access
Licence
Locations
  • The ISME Journal (publishedVersion, cc-by-nc)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • VBN Forskningsportal (Aalborg Universitet) (publishedVersion)
  • Montana State University ScholarWorks (Montana State University) (submittedVersion, cc-by)
Funders
  • NASA | NASA Astrobiology Institute (NNA15BB02A)
  • National Science Foundation (OIA-1826734, OCE-1335810)
Topics
  • Physical Sciences › Environmental Science › Environmental Chemistry › Methane Hydrates and Related Phenomena
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Microbial metabolism and enzyme function
  • Physical Sciences › Environmental Science › Ecology › Microbial Community Ecology and Physiology
Keywords
methanogenic archaea, Methanobacterium, serpentinization, hydrogenotrophic methanogenesis, formate dehydrogenase, [NiFe] hydrogenase, Samail ophiolite, metagenome-assembled genomes, single amplified genomes, gene transfer, methane production
MeSH terms
Methane, Oman, Phylogeny, Oxidants, Euryarchaeota

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review