Syntrophic entanglements for propionate and acetate oxidation under thermophilic and high-ammonia conditions.


Journal

The ISME journal
ISSN: 1751-7370
Titre abrégé: ISME J
Pays: England
ID NLM: 101301086

Informations de publication

Date de publication:
11 2023
Historique:
received: 17 03 2023
accepted: 25 08 2023
revised: 22 08 2023
medline: 23 10 2023
pubmed: 8 9 2023
entrez: 7 9 2023
Statut: ppublish

Résumé

Propionate is a key intermediate in anaerobic digestion processes and often accumulates in association with perturbations, such as elevated levels of ammonia. Under such conditions, syntrophic ammonia-tolerant microorganisms play a key role in propionate degradation. Despite their importance, little is known about these syntrophic microorganisms and their cross-species interactions. Here, we present metagenomes and metatranscriptomic data for novel thermophilic and ammonia-tolerant syntrophic bacteria and the partner methanogens enriched in propionate-fed reactors. A metagenome for a novel bacterium for which we propose the provisional name 'Candidatus Thermosyntrophopropionicum ammoniitolerans' was recovered, together with mapping of its highly expressed methylmalonyl-CoA pathway for syntrophic propionate degradation. Acetate was degraded by a novel thermophilic syntrophic acetate-oxidising candidate bacterium. Electron removal associated with syntrophic propionate and acetate oxidation was mediated by the hydrogen/formate-utilising methanogens Methanoculleus sp. and Methanothermobacter sp., with the latter observed to be critical for efficient propionate degradation. Similar dependence on Methanothermobacter was not seen for acetate degradation. Expression-based analyses indicated use of both H

Identifiants

pubmed: 37679429
doi: 10.1038/s41396-023-01504-y
pii: 10.1038/s41396-023-01504-y
pmc: PMC10579422
doi:

Substances chimiques

Propionates 0
Ammonia 7664-41-7
Acetates 0
Formates 0
Hydrogen 7YNJ3PO35Z
Methane OP0UW79H66

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

1966-1978

Informations de copyright

© 2023. The Author(s).

Références

Nat Biotechnol. 2020 Sep;38(9):1079-1086
pubmed: 32341564
Int J Mol Sci. 2020 Nov 20;21(22):
pubmed: 33233586
FEMS Microbiol Rev. 2022 Mar 3;46(2):
pubmed: 34875063
Bioresour Technol. 2018 Feb;250:117-123
pubmed: 29161570
J Dairy Sci. 2000 Dec;83(12):2740-6
pubmed: 11132840
Microbes Environ. 2010;25(3):145-51
pubmed: 21576866
Environ Microbiol. 2018 Dec;20(12):4503-4511
pubmed: 30126076
J Bacteriol. 2015 May;197(9):1681-9
pubmed: 25733614
Annu Rev Microbiol. 2012;66:429-52
pubmed: 22803797
Appl Microbiol Biotechnol. 2015 Aug;99(15):6215-29
pubmed: 26142387
Water Res. 2002 Oct;36(17):4369-85
pubmed: 12420941
Microb Biotechnol. 2009 Sep;2(5):575-84
pubmed: 21255290
Eur J Biochem. 2003 Jun;270(11):2476-85
pubmed: 12755703
Stand Genomic Sci. 2013 Apr 15;8(1):69-87
pubmed: 23961313
Bioresour Technol. 2014 Oct;169:502-509
pubmed: 25086435
J Bacteriol. 2009 Jul;191(13):4451-7
pubmed: 19411328
Appl Microbiol Biotechnol. 1998 Oct;50(4):495-501
pubmed: 9830101
Appl Environ Microbiol. 2000 Jul;66(7):2934-42
pubmed: 10877789
Philos Trans R Soc Lond B Biol Sci. 2008 Jun 27;363(1500):2135-42
pubmed: 18339602
Mol Microbiol. 2001 Dec;42(5):1199-209
pubmed: 11886552
Int J Syst Bacteriol. 1996 Oct;46(4):1145-52
pubmed: 8863449
Appl Environ Microbiol. 2005 Dec;71(12):7838-45
pubmed: 16332758
Curr Opin Struct Biol. 2000 Dec;10(6):672-9
pubmed: 11114504
Nat Methods. 2016 Jul;13(7):581-3
pubmed: 27214047
Dev Cell. 2016 Feb 22;36(4):453-61
pubmed: 26906740
Science. 2009 Mar 20;323(5921):1574
pubmed: 19299611
Proc Natl Acad Sci U S A. 2006 Jul 25;103(30):11358-63
pubmed: 16849424
PLoS One. 2013 Apr 22;8(4):e61217
pubmed: 23630581
Nat Rev Microbiol. 2011 Jun;9(6):452-66
pubmed: 21572460
Nucleic Acids Res. 2015 Aug 18;43(14):6761-71
pubmed: 26150420
Genome Biol. 2014;15(12):550
pubmed: 25516281
Adv Biochem Eng Biotechnol. 2003;81:95-150
pubmed: 12747562
Curr Opin Microbiol. 2009 Dec;12(6):667-73
pubmed: 19854099
ISME J. 2020 Apr;14(4):906-918
pubmed: 31896784
Microb Ecol. 2017 May;73(4):916-924
pubmed: 27815590
PLoS One. 2012;7(12):e50527
pubmed: 23236376
Water Res. 2018 Dec 1;146:275-287
pubmed: 30278382
Curr Opin Microbiol. 2018 Apr;42:1-6
pubmed: 28961452
Science. 2015 Dec 18;350(6267):1541-5
pubmed: 26680199
Water Res. 2016 Nov 15;105:314-319
pubmed: 27639056
Chemosphere. 2020 Sep;255:126840
pubmed: 32387725
Microb Genom. 2021 Nov;7(11):
pubmed: 34739369
Environ Microbiol. 2016 Sep;18(9):2797-809
pubmed: 27376701
Genome Res. 2017 May;27(5):737-746
pubmed: 28100585
Microb Biotechnol. 2018 Jul;11(4):680-693
pubmed: 29239113
Arch Biochem Biophys. 2008 Aug 1;476(1):43-50
pubmed: 18515057
Microb Ecol. 1977 Sep;4(3):241-8
pubmed: 24232163
Appl Biochem Biotechnol. 2019 Sep;189(1):233-248
pubmed: 30972704
World J Microbiol Biotechnol. 2020 Oct 1;36(11):165
pubmed: 33000364
Appl Environ Microbiol. 2015 Aug;81(15):5223-34
pubmed: 26025891
Nat Commun. 2015 Feb 23;6:6283
pubmed: 25704114
FEMS Microbiol Lett. 2015 Jan;362(3):1-7
pubmed: 25673652
J Bacteriol. 2006 Jan;188(1):202-10
pubmed: 16352836
Front Microbiol. 2018 Nov 30;9:2921
pubmed: 30555446
Nat Biotechnol. 2019 May;37(5):540-546
pubmed: 30936562
Appl Microbiol Biotechnol. 2013 Sep;97(17):7699-709
pubmed: 23250223
Appl Environ Microbiol. 1988 Jun;54(6):1457-61
pubmed: 16347656
Mol Microbiol. 1998 Jul;29(1):321-30
pubmed: 9701824
Antonie Van Leeuwenhoek. 2002 Aug;81(1-4):283-91
pubmed: 12448727
Environ Microbiol Rep. 2011 Aug;3(4):500-5
pubmed: 23761313
Nucleic Acids Res. 2022 Jan 7;50(D1):D801-D807
pubmed: 34634793
J Bacteriol. 2014 Jan;196(2):265-75
pubmed: 24163345
Int J Syst Evol Microbiol. 2002 Jan;52(Pt 1):157-164
pubmed: 11837298
Environ Microbiol. 2021 Mar;23(3):1620-1637
pubmed: 33400377
Environ Pollut. 2020 Oct;265(Pt B):114843
pubmed: 32480003
Eur J Biochem. 2002 Dec;269(24):6184-94
pubmed: 12473114
Environ Microbiol Rep. 2010 Aug;2(4):489-99
pubmed: 23766220
J Bacteriol. 2010 Feb;192(4):994-1010
pubmed: 20008072
Environ Int. 2020 May;138:105650
pubmed: 32182450
Front Microbiol. 2018 Dec 04;9:2911
pubmed: 30564206
Bioresour Technol. 2018 May;256:44-52
pubmed: 29428613
Bioresour Technol. 2008 Jan;99(1):170-8
pubmed: 17197176
PLoS One. 2016 Nov 16;11(11):e0166520
pubmed: 27851830
Microb Ecol. 2020 Jul;80(1):120-132
pubmed: 31982930
Genome Biol. 2019 Nov 14;20(1):238
pubmed: 31727128
Arch Microbiol. 1997 Nov;168(5):396-402
pubmed: 9325428
Nat Rev Microbiol. 2009 Aug;7(8):568-77
pubmed: 19609258
Stand Genomic Sci. 2016 Oct 12;11:80
pubmed: 27777650
FEMS Microbiol Lett. 2010 Aug 1;309(1):100-4
pubmed: 20546311
Int J Syst Evol Microbiol. 2016 Mar;66(3):1506-1509
pubmed: 26791251
Int J Syst Evol Microbiol. 2002 Sep;52(Pt 5):1729-1735
pubmed: 12361280
Int J Syst Evol Microbiol. 2007 Jan;57(Pt 1):81-91
pubmed: 17220447
Genome Res. 2015 Jul;25(7):1043-55
pubmed: 25977477
Microbiol Rev. 1989 Mar;53(1):121-47
pubmed: 2651863
Chemosphere. 1997 Oct;35(7):1487-95
pubmed: 9314189
Environ Microbiol Rep. 2019 Aug;11(4):558-570
pubmed: 30985964
Bioresour Technol. 2020 May;304:122981
pubmed: 32088624
Front Microbiol. 2019 Mar 19;10:423
pubmed: 30949135
J Biosci Bioeng. 2001;91(3):294-8
pubmed: 16232992
Front Bioeng Biotechnol. 2020 Dec 11;8:604838
pubmed: 33363133
Environ Microbiol. 2018 May;20(5):1842-1856
pubmed: 29611893
Sci Rep. 2016 Sep 27;6:34212
pubmed: 27670643
PLoS One. 2014 Nov 19;9(11):e112963
pubmed: 25409509
Int J Syst Bacteriol. 1997 Jan;47(1):150-4
pubmed: 8995817
Appl Environ Microbiol. 2013 Oct;79(19):6176-9
pubmed: 23872566
Environ Sci Technol. 2019 May 7;53(9):5512-5520
pubmed: 30990997
Nat Methods. 2017 Apr;14(4):417-419
pubmed: 28263959
Bioinformatics. 2019 Nov 15;:
pubmed: 31730192
Adv Microb Physiol. 1998;40:81-136
pubmed: 9889977
Microb Biotechnol. 2021 Mar;14(2):386-391
pubmed: 32476222
Genome Biol. 2019 Nov 28;20(1):257
pubmed: 31779668
FEMS Microbiol Ecol. 2008 Sep;65(3):544-54
pubmed: 18647356
Methods Enzymol. 2017;595:185-212
pubmed: 28882201
Bioinformatics. 2014 Jul 15;30(14):2068-9
pubmed: 24642063
Microbiome. 2018 Sep 15;6(1):158
pubmed: 30219103
Biotechnol Bioeng. 2005 Mar 20;89(6):670-9
pubmed: 15696537
Nat Commun. 2015 Feb 23;6:6238
pubmed: 25703793
Biochim Biophys Acta. 2014 Jul;1837(7):1148-64
pubmed: 24662917
J Bacteriol. 2008 Apr;190(7):2572-9
pubmed: 18245282
Proc Natl Acad Sci U S A. 2016 Dec 27;113(52):E8396-E8405
pubmed: 27956617
Front Microbiol. 2018 Jul 09;9:1551
pubmed: 30038609

Auteurs

Abhijeet Singh (A)

Department of Molecular Sciences, Swedish University of Agricultural Sciences, SE-750 07, Uppsala, Sweden.

Anna Schnürer (A)

Department of Molecular Sciences, Swedish University of Agricultural Sciences, SE-750 07, Uppsala, Sweden.

Jan Dolfing (J)

Faculty of Energy and Environment, Northumbria University, Newcastle-upon-Tyne, NE18QH, UK.

Maria Westerholm (M)

Department of Molecular Sciences, Swedish University of Agricultural Sciences, SE-750 07, Uppsala, Sweden. maria.westerholm@slu.se.

Articles similaires

Populus Soil Microbiology Soil Microbiota Fungi
Aerosols Humans Decontamination Air Microbiology Masks
Coal Metagenome Phylogeny Bacteria Genome, Bacterial
Semiconductors Photosynthesis Polymers Carbon Dioxide Bacteria

Classifications MeSH