Deep-sea Bacteroidetes from the Mariana Trench specialize in hemicellulose and pectin degradation typically associated with terrestrial systems.
Bacteroidetes
Cell wall polysaccharide utilization
Hadal trench
Metagenomics
Sinking debris
Journal
Microbiome
ISSN: 2049-2618
Titre abrégé: Microbiome
Pays: England
ID NLM: 101615147
Informations de publication
Date de publication:
07 08 2023
07 08 2023
Historique:
received:
07
06
2023
accepted:
11
07
2023
medline:
9
8
2023
pubmed:
8
8
2023
entrez:
7
8
2023
Statut:
epublish
Résumé
Hadal trenches (>6000 m) are the deepest oceanic regions on Earth and depocenters for organic materials. However, how these enigmatic microbial ecosystems are fueled is largely unknown, particularly the proportional importance of complex polysaccharides introduced through deposition from the photic surface waters above. In surface waters, Bacteroidetes are keystone taxa for the cycling of various algal-derived polysaccharides and the flux of carbon through the photic zone. However, their role in the hadal microbial loop is almost unknown. Here, culture-dependent and culture-independent methods were used to study the potential of Bacteroidetes to catabolize diverse polysaccharides in Mariana Trench waters. Compared to surface waters, the bathypelagic (1000-4000 m) and hadal (6000-10,500 m) waters harbored distinct Bacteroidetes communities, with Mesoflavibacter being enriched at ≥ 4000 m and Bacteroides and Provotella being enriched at 10,400-10,500 m. Moreover, these deep-sea communities possessed distinct gene pools encoding for carbohydrate active enzymes (CAZymes), suggesting different polysaccharide sources are utilised in these two zones. Compared to surface counterparts, deep-sea Bacteroidetes showed significant enrichment of CAZyme genes frequently organized into polysaccharide utilization loci (PULs) targeting algal/plant cell wall polysaccharides (i.e., hemicellulose and pectin), that were previously considered an ecological trait associated with terrestrial Bacteroidetes only. Using a hadal Mesoflavibacter isolate (MTRN7), functional validation of this unique genetic potential was demonstrated. MTRN7 could utilize pectic arabinans, typically associated with land plants and phototrophic algae, as the carbon source under simulated deep-sea conditions. Interestingly, a PUL we demonstrate is likely horizontally acquired from coastal/land Bacteroidetes was activated during growth on arabinan and experimentally shown to encode enzymes that hydrolyze arabinan at depth. Our study implies that hadal Bacteroidetes exploit polysaccharides poorly utilized by surface populations via an expanded CAZyme gene pool. We propose that sinking cell wall debris produced in the photic zone can serve as an important carbon source for hadal heterotrophs and play a role in shaping their communities and metabolism. Video Abstract.
Sections du résumé
BACKGROUND
Hadal trenches (>6000 m) are the deepest oceanic regions on Earth and depocenters for organic materials. However, how these enigmatic microbial ecosystems are fueled is largely unknown, particularly the proportional importance of complex polysaccharides introduced through deposition from the photic surface waters above. In surface waters, Bacteroidetes are keystone taxa for the cycling of various algal-derived polysaccharides and the flux of carbon through the photic zone. However, their role in the hadal microbial loop is almost unknown.
RESULTS
Here, culture-dependent and culture-independent methods were used to study the potential of Bacteroidetes to catabolize diverse polysaccharides in Mariana Trench waters. Compared to surface waters, the bathypelagic (1000-4000 m) and hadal (6000-10,500 m) waters harbored distinct Bacteroidetes communities, with Mesoflavibacter being enriched at ≥ 4000 m and Bacteroides and Provotella being enriched at 10,400-10,500 m. Moreover, these deep-sea communities possessed distinct gene pools encoding for carbohydrate active enzymes (CAZymes), suggesting different polysaccharide sources are utilised in these two zones. Compared to surface counterparts, deep-sea Bacteroidetes showed significant enrichment of CAZyme genes frequently organized into polysaccharide utilization loci (PULs) targeting algal/plant cell wall polysaccharides (i.e., hemicellulose and pectin), that were previously considered an ecological trait associated with terrestrial Bacteroidetes only. Using a hadal Mesoflavibacter isolate (MTRN7), functional validation of this unique genetic potential was demonstrated. MTRN7 could utilize pectic arabinans, typically associated with land plants and phototrophic algae, as the carbon source under simulated deep-sea conditions. Interestingly, a PUL we demonstrate is likely horizontally acquired from coastal/land Bacteroidetes was activated during growth on arabinan and experimentally shown to encode enzymes that hydrolyze arabinan at depth.
CONCLUSIONS
Our study implies that hadal Bacteroidetes exploit polysaccharides poorly utilized by surface populations via an expanded CAZyme gene pool. We propose that sinking cell wall debris produced in the photic zone can serve as an important carbon source for hadal heterotrophs and play a role in shaping their communities and metabolism. Video Abstract.
Identifiants
pubmed: 37550707
doi: 10.1186/s40168-023-01618-7
pii: 10.1186/s40168-023-01618-7
pmc: PMC10405439
doi:
Substances chimiques
hemicellulose
8024-50-8
Polysaccharides
0
Pectins
89NA02M4RX
Types de publication
Video-Audio Media
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
175Subventions
Organisme : Biotechnology and Biological Sciences Research Council
ID : BB/X005968
Pays : United Kingdom
Informations de copyright
© 2023. BioMed Central Ltd., part of Springer Nature.
Références
Environ Microbiol. 2017 Jun;19(6):2320-2333
pubmed: 28276126
Appl Environ Microbiol. 2017 Aug 31;83(18):
pubmed: 28710263
PLoS Comput Biol. 2016 Jun 21;12(6):e1004957
pubmed: 27327495
PLoS Comput Biol. 2017 Jun 8;13(6):e1005595
pubmed: 28594827
Bioinformatics. 2010 Jan 1;26(1):139-40
pubmed: 19910308
BMC Bioinformatics. 2010 Mar 08;11:119
pubmed: 20211023
ISME J. 2015 Jun;9(6):1410-22
pubmed: 25478683
Nat Commun. 2020 Sep 16;11(1):4658
pubmed: 32938931
ISME J. 2020 Jun;14(6):1369-1383
pubmed: 32071394
ISME J. 2022 Mar;16(3):630-641
pubmed: 34493810
Microbiome. 2022 May 10;10(1):75
pubmed: 35538590
Nat Commun. 2019 May 3;10(1):2043
pubmed: 31053724
Environ Microbiol. 2016 Dec;18(12):4610-4627
pubmed: 27768819
Elife. 2016 Apr 07;5:e11888
pubmed: 27054497
ISME J. 2021 Apr;15(4):1040-1055
pubmed: 33257812
ISME J. 2019 Jan;13(1):76-91
pubmed: 30111868
Trends Ecol Evol. 2010 Mar;25(3):190-7
pubmed: 19846236
Nat Commun. 2021 Feb 19;12(1):1150
pubmed: 33608542
Bioinformatics. 2014 Aug 1;30(15):2114-20
pubmed: 24695404
ISME J. 2019 Nov;13(11):2800-2816
pubmed: 31316134
Proc Natl Acad Sci U S A. 2012 Nov 27;109(48):19786-91
pubmed: 23150581
Nat Biotechnol. 2018 Apr;36(4):359-367
pubmed: 29553575
Nucleic Acids Res. 2021 Jan 8;49(D1):D523-D528
pubmed: 32941621
Annu Rev Plant Biol. 2011;62:567-90
pubmed: 21351878
Ann Rev Mar Sci. 2021 Jan;13:81-108
pubmed: 32726567
Front Microbiol. 2021 Jan 18;11:603692
pubmed: 33537012
Environ Microbiol. 2019 Feb;21(2):716-729
pubmed: 30592124
ISME Commun. 2021 Sep 29;1(1):51
pubmed: 36747039
Methods. 2016 Jun 1;102:3-11
pubmed: 27012178
Nucleic Acids Res. 2021 Jul 2;49(W1):W293-W296
pubmed: 33885785
mBio. 2016 Oct 11;7(5):
pubmed: 27729509
Environ Microbiol. 2019 Feb;21(2):648-666
pubmed: 30565818
mSystems. 2020 Oct 27;5(5):
pubmed: 33109753
BMC Bioinformatics. 2011 Aug 04;12:323
pubmed: 21816040
Front Microbiol. 2016 Aug 10;7:1261
pubmed: 27559333
ISME J. 2023 Feb;17(2):276-285
pubmed: 36411326
J Biol Chem. 2006 Nov 24;281(47):36269-79
pubmed: 16968696
Nat Methods. 2012 Mar 04;9(4):357-9
pubmed: 22388286
PLoS One. 2018 Apr 5;13(4):e0195102
pubmed: 29621268
Nat Rev Microbiol. 2021 Sep;19(9):585-599
pubmed: 34050328
Curr Microbiol. 2018 Sep;75(9):1142-1146
pubmed: 29696370
Microorganisms. 2020 Aug 27;8(9):
pubmed: 32867361
Mar Genomics. 2016 Feb;25:115-121
pubmed: 26795059
Genome Res. 2015 Jul;25(7):1043-55
pubmed: 25977477
Sci Adv. 2020 Apr 15;6(16):eaaz4354
pubmed: 32494615
Bioinformatics. 2009 Aug 1;25(15):1972-3
pubmed: 19505945
Microbiome. 2022 Dec 7;10(1):215
pubmed: 36476562
Genome Biol. 2021 Jul 13;22(1):207
pubmed: 34256809
PLoS One. 2010 Mar 10;5(3):e9490
pubmed: 20224823
Brief Bioinform. 2019 Jul 19;20(4):1160-1166
pubmed: 28968734
Microbiome. 2020 Jun 1;8(1):78
pubmed: 32482169
Environ Microbiol. 2021 Aug;23(8):4561-4575
pubmed: 34196089
Nature. 2010 Apr 8;464(7290):908-12
pubmed: 20376150
Proc Natl Acad Sci U S A. 2015 Mar 17;112(11):E1230-6
pubmed: 25713387
ISME J. 2013 May;7(5):1026-37
pubmed: 23303374
PLoS One. 2011;6(12):e28900
pubmed: 22216139
Science. 2012 May 4;336(6081):608-11
pubmed: 22556258
Science. 2015 May 22;348(6237):1261359
pubmed: 25999513
Nat Rev Microbiol. 2008 Feb;6(2):121-31
pubmed: 18180751
Nat Commun. 2022 Mar 21;13(1):1515
pubmed: 35314706
Bioinformatics. 2019 Nov 15;:
pubmed: 31730192
Nucleic Acids Res. 2018 Jan 4;46(D1):D624-D632
pubmed: 29145643
PLoS One. 2012;7(8):e42727
pubmed: 22905166
Nucleic Acids Res. 2007;35(9):3100-8
pubmed: 17452365
Microbiome. 2019 Apr 12;7(1):47
pubmed: 30975208
Bioinformatics. 2014 Jul 15;30(14):2068-9
pubmed: 24642063
PLoS One. 2016 Oct 17;11(10):e0164846
pubmed: 27749924
Nat Microbiol. 2018 Jul;3(7):804-813
pubmed: 29891866
Nucleic Acids Res. 2018 Jul 2;46(W1):W95-W101
pubmed: 29771380