Physiological potential and evolutionary trajectories of syntrophic sulfate-reducing bacterial partners of anaerobic methanotrophic archaea.
Journal
PLoS biology
ISSN: 1545-7885
Titre abrégé: PLoS Biol
Pays: United States
ID NLM: 101183755
Informations de publication
Date de publication:
09 2023
09 2023
Historique:
received:
23
11
2022
accepted:
08
08
2023
revised:
05
10
2023
medline:
9
10
2023
pubmed:
25
9
2023
entrez:
25
9
2023
Statut:
epublish
Résumé
Sulfate-coupled anaerobic oxidation of methane (AOM) is performed by multicellular consortia of anaerobic methanotrophic archaea (ANME) in obligate syntrophic partnership with sulfate-reducing bacteria (SRB). Diverse ANME and SRB clades co-associate but the physiological basis for their adaptation and diversification is not well understood. In this work, we used comparative metagenomics and phylogenetics to investigate the metabolic adaptation among the 4 main syntrophic SRB clades (HotSeep-1, Seep-SRB2, Seep-SRB1a, and Seep-SRB1g) and identified features associated with their syntrophic lifestyle that distinguish them from their non-syntrophic evolutionary neighbors in the phylum Desulfobacterota. We show that the protein complexes involved in direct interspecies electron transfer (DIET) from ANME to the SRB outer membrane are conserved between the syntrophic lineages. In contrast, the proteins involved in electron transfer within the SRB inner membrane differ between clades, indicative of convergent evolution in the adaptation to a syntrophic lifestyle. Our analysis suggests that in most cases, this adaptation likely occurred after the acquisition of the DIET complexes in an ancestral clade and involve horizontal gene transfers within pathways for electron transfer (CbcBA) and biofilm formation (Pel). We also provide evidence for unique adaptations within syntrophic SRB clades, which vary depending on the archaeal partner. Among the most widespread syntrophic SRB, Seep-SRB1a, subclades that specifically partner ANME-2a are missing the cobalamin synthesis pathway, suggestive of nutritional dependency on its partner, while closely related Seep-SRB1a partners of ANME-2c lack nutritional auxotrophies. Our work provides insight into the features associated with DIET-based syntrophy and the adaptation of SRB towards it.
Identifiants
pubmed: 37747940
doi: 10.1371/journal.pbio.3002292
pii: PBIOLOGY-D-22-02613
pmc: PMC10553843
doi:
Substances chimiques
Sulfates
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
e3002292Informations de copyright
Copyright: This is an open access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication.
Déclaration de conflit d'intérêts
The authors have declared that no competing interests exist.
Références
Environ Microbiol. 2014 Oct;16(10):3012-29
pubmed: 24107237
Proc Natl Acad Sci U S A. 2009 Nov 10;106(45):19126-31
pubmed: 19855009
mSystems. 2017 Oct 31;2(5):
pubmed: 29104938
ISME J. 2022 Jan;16(1):168-177
pubmed: 34285362
Science. 2014 Jan 31;343(6170):529-33
pubmed: 24407482
PeerJ. 2019 Jul 26;7:e7359
pubmed: 31388474
Nat Struct Biol. 1998 Nov;5(11):1005-12
pubmed: 9808046
BMC Genomics. 2012 May 03;13:162
pubmed: 22554235
Trends Microbiol. 2013 Feb;21(2):63-72
pubmed: 23117123
Cell Rep. 2019 Oct 8;29(2):511-521.e2
pubmed: 31597107
Proc Natl Acad Sci U S A. 2002 May 28;99(11):7663-8
pubmed: 12032340
Nucleic Acids Res. 2021 Jan 8;49(D1):D1020-D1028
pubmed: 33270901
mBio. 2017 Aug 1;8(4):
pubmed: 28765215
ISME J. 2020 May;14(5):1260-1272
pubmed: 32047278
Nucleic Acids Res. 2020 Jan 8;48(D1):D265-D268
pubmed: 31777944
Virulence. 2010 Nov-Dec;1(6):541-5
pubmed: 21178499
Appl Environ Microbiol. 2014 Feb;80(3):855-68
pubmed: 24242254
Cell. 2019 Apr 4;177(2):361-369.e10
pubmed: 30951668
Environ Microbiol. 2016 Sep;18(9):3073-91
pubmed: 26971539
Nature. 2000 Oct 5;407(6804):623-6
pubmed: 11034209
PLoS One. 2011;6(10):e26161
pubmed: 22028825
Sci Rep. 2014 Jul 16;4:5696
pubmed: 25027246
Science. 2012 Jul 13;337(6091):236-9
pubmed: 22798614
Science. 2001 Jul 20;293(5529):484-7
pubmed: 11463914
Nat Biotechnol. 2018 Nov;36(10):996-1004
pubmed: 30148503
mBio. 2021 May 11;12(3):
pubmed: 33975943
Front Microbiol. 2011 Aug 22;2:167
pubmed: 21991261
Nature. 2015 Oct 22;526(7574):587-90
pubmed: 26490622
Front Microbiol. 2016 Apr 27;7:598
pubmed: 27199928
ISME J. 2014 May;8(5):1069-78
pubmed: 24335827
Nucleic Acids Res. 2004 Jul 1;32(Web Server issue):W400-4
pubmed: 15215419
PeerJ. 2016 Apr 18;4:e1913
pubmed: 27114874
J Bacteriol. 2020 Mar 26;202(8):
pubmed: 31988082
Bioinformatics. 2014 May 1;30(9):1312-3
pubmed: 24451623
J Bacteriol. 2011 Mar;193(5):1023-33
pubmed: 21169487
Environ Microbiol. 2010 Aug;12(8):2327-40
pubmed: 21966923
Science. 2002 Aug 9;297(5583):1013-5
pubmed: 12169733
Nat Commun. 2018 Nov 27;9(1):4999
pubmed: 30479325
Environ Microbiol. 2018 May;20(5):1651-1666
pubmed: 29468803
Nature. 1999 Apr 29;398(6730):802-5
pubmed: 10235261
PLoS Biol. 2022 Jan 5;20(1):e3001508
pubmed: 34986141
Environ Microbiol. 2008 Aug;10(8):1934-47
pubmed: 18430014
Int J Syst Evol Microbiol. 2014 Feb;64(Pt 2):346-351
pubmed: 24505072
Microbiome. 2015 Apr 13;3:14
pubmed: 25922666
Appl Environ Microbiol. 2002 Apr;68(4):1994-2007
pubmed: 11916723
Nat Microbiol. 2017 Nov;2(11):1533-1542
pubmed: 28894102
J Bacteriol. 2015 Mar 30;197(13):2092-2103
pubmed: 25825428
Commun Biol. 2020 Aug 7;3(1):431
pubmed: 32770029
Environ Microbiol. 2010 Feb;12(2):422-39
pubmed: 19878267
Appl Environ Microbiol. 2007 May;73(10):3348-62
pubmed: 17369343
Front Microbiol. 2015 May 13;6:477
pubmed: 26029201
Bioinformatics. 2010 Oct 1;26(19):2460-1
pubmed: 20709691
Annu Rev Microbiol. 2009;63:311-34
pubmed: 19575572
mBio. 2016 May 24;7(3):
pubmed: 27222468
ISME J. 2016 Mar;10(3):678-92
pubmed: 26394007
Geobiology. 2014 May;12(3):221-30
pubmed: 24730641
Nature. 2021 Aug;596(7873):583-589
pubmed: 34265844
Microb Ecol. 2001 Jul;42(1):1-10
pubmed: 12035076
Proc Natl Acad Sci U S A. 2008 May 13;105(19):7052-7
pubmed: 18467493
Appl Environ Microbiol. 2001 Apr;67(4):1922-34
pubmed: 11282650
ISME J. 2021 Feb;15(2):377-396
pubmed: 33060828
Environ Microbiol. 2015 Jul;17(7):2288-305
pubmed: 25367508
Mol Biol Evol. 2016 Nov;33(11):2874-2884
pubmed: 27501943
Cell Metab. 2014 Nov 4;20(5):769-778
pubmed: 25440056
J Bacteriol. 1999 Mar;181(5):1496-507
pubmed: 10049381
ISME J. 2019 Mar;13(3):789-804
pubmed: 30429574
PLoS Pathog. 2018 May 18;14(5):e1007074
pubmed: 29775484
mBio. 2020 Oct 20;11(5):
pubmed: 33082256
FEMS Microbiol Rev. 2013 May;37(3):384-406
pubmed: 23480449
Environ Microbiol. 2023 May;25(5):962-976
pubmed: 36602077
Bioinformatics. 2007 Jan 1;23(1):127-8
pubmed: 17050570
Nat Microbiol. 2021 Jan;6(1):3-6
pubmed: 33349678
Nat Biotechnol. 2019 Apr;37(4):420-423
pubmed: 30778233
Mol Microbiol. 1998 Oct;30(2):275-84
pubmed: 9791173
Nat Commun. 2020 Aug 7;11(1):3941
pubmed: 32770005
Annu Rev Microbiol. 2022 Sep 8;76:553-577
pubmed: 35917471
Protein Sci. 2020 Apr;29(4):830-842
pubmed: 31721352
Proc Natl Acad Sci U S A. 2015 Mar 31;112(13):4015-20
pubmed: 25775520
ISME J. 2014 Jan;8(1):150-63
pubmed: 24008326
Appl Environ Microbiol. 2018 May 17;84(11):
pubmed: 29625978
mBio. 2020 Apr 21;11(2):
pubmed: 32317322
Biochim Biophys Acta Bioenerg. 2021 Apr 1;1862(4):148379
pubmed: 33460586
Appl Environ Microbiol. 2022 Jun 14;88(11):e0210921
pubmed: 35604226
Sci Rep. 2021 Feb 26;11(1):4763
pubmed: 33637779
Cell. 2019 Apr 4;177(2):370-383.e15
pubmed: 30905475
Proc Natl Acad Sci U S A. 2015 Aug 25;112(34):10792-7
pubmed: 26246619
Int J Syst Evol Microbiol. 2016 Jul;66(7):2515-2519
pubmed: 27082267
Microb Genom. 2020 Jul;6(7):
pubmed: 32553052
ISME J. 2022 Jul;16(7):1750-1764
pubmed: 35352015
Mol Biol Evol. 2020 May 1;37(5):1530-1534
pubmed: 32011700
BMC Bioinformatics. 2010 Aug 18;11:431
pubmed: 20718988
J Comput Biol. 2012 May;19(5):455-77
pubmed: 22506599
Mol Microbiol. 2021 Oct;116(4):1124-1139
pubmed: 34423503
Nature. 2019 Apr;568(7750):108-111
pubmed: 30918404
ISME J. 2022 Jan;16(1):307-320
pubmed: 34331018
Bioinformatics. 2009 May 1;25(9):1189-91
pubmed: 19151095
Nature. 2016 Nov 17;539(7629):396-401
pubmed: 27749816
Chem Rev. 2021 Feb 10;121(3):1804-1844
pubmed: 33398986
J Bacteriol. 2005 Sep;187(17):5918-26
pubmed: 16109933
Nucleic Acids Res. 2021 Jan 8;49(D1):D412-D419
pubmed: 33125078
J Am Chem Soc. 2022 Apr 20;144(15):6791-6801
pubmed: 35380814
Curr Opin Microbiol. 2009 Jun;12(3):231-7
pubmed: 19447672
Nature. 2006 Oct 19;443(7113):854-8
pubmed: 17051217
Proc Natl Acad Sci U S A. 2003 Apr 29;100(9):5443-8
pubmed: 12704238
FEMS Microbiol Ecol. 2020 Nov 3;96(11):
pubmed: 32520336
Appl Environ Microbiol. 1996 Feb;62(2):316-22
pubmed: 8593035
Sci Total Environ. 2020 Nov 1;741:140365
pubmed: 32610234
Front Microbiol. 2017 Nov 23;8:2325
pubmed: 29218041
BMC Bioinformatics. 2004 Aug 19;5:113
pubmed: 15318951
Genome Res. 2015 Jul;25(7):1043-55
pubmed: 25977477
J Bacteriol. 2020 Sep 8;202(19):
pubmed: 32778557
Microbiol Mol Biol Rev. 1997 Jun;61(2):262-80
pubmed: 9184013
Nature. 2015 Oct 22;526(7574):531-5
pubmed: 26375009
Front Microbiol. 2016 Mar 31;7:374
pubmed: 27065954
Science. 2009 Oct 16;326(5951):422-6
pubmed: 19833965
Front Microbiol. 2011 Apr 19;2:69
pubmed: 21747791
Sci Rep. 2019 Jul 5;9(1):9725
pubmed: 31278352
Int J Mol Sci. 2018 Mar 11;19(3):
pubmed: 29534491
Microb Cell Fact. 2017 Jan 30;16(1):15
pubmed: 28137297
Nucleic Acids Res. 2000 Jan 1;28(1):27-30
pubmed: 10592173
Appl Environ Microbiol. 2005 Jan;71(1):467-79
pubmed: 15640223
J Bacteriol. 2018 Sep 10;200(19):
pubmed: 30038047
J Bacteriol. 2013 Sep;195(17):3987-94
pubmed: 23836862
Microbes Environ. 2013;28(1):141-8
pubmed: 23363619
Environ Microbiol. 2022 Apr;24(4):1964-1976
pubmed: 35257474
Nat Biotechnol. 2018 Jul 6;36(7):566-569
pubmed: 29979655
Ann Rev Mar Sci. 2011;3:261-89
pubmed: 21329206
Bioinformatics. 2019 Nov 15;:
pubmed: 31730192
Nat Commun. 2018 Dec 21;9(1):5448
pubmed: 30575735
Int J Syst Evol Microbiol. 2013 Jun;63(Pt 6):1967-1971
pubmed: 23024145
Biol Direct. 2007 Nov 27;2:33
pubmed: 18042280
Microbiology (Reading). 2013 Mar;159(Pt 3):515-535
pubmed: 23306674
Front Microbiol. 2014 Oct 31;5:577
pubmed: 25400629
Nat Rev Microbiol. 2018 Jun;16(6):383-390
pubmed: 29599459
Proc Natl Acad Sci U S A. 2015 Sep 8;112(36):11353-8
pubmed: 26311845
Bioinformatics. 2014 Jul 15;30(14):2068-9
pubmed: 24642063
Front Microbiol. 2018 Mar 14;9:401
pubmed: 29593673
Nature. 2005 Nov 3;438(7064):90-3
pubmed: 16267554
Biochim Biophys Acta. 2014 Jul;1837(7):1148-64
pubmed: 24662917
Bioinformatics. 2020 Apr 1;36(7):2251-2252
pubmed: 31742321
Nucleic Acids Res. 2003 Jan 1;31(1):371-3
pubmed: 12520025
J Bacteriol. 2017 Oct 3;199(21):
pubmed: 28808132
Bioinformatics. 2010 Jun 15;26(12):1481-7
pubmed: 20439257
Mol Microbiol. 2000 Feb;35(3):686-96
pubmed: 10672190
Proc Natl Acad Sci U S A. 2016 Jul 12;113(28):E4069-78
pubmed: 27357680