Dissolved storage glycans shaped the community composition of abundant bacterioplankton clades during a North Sea spring phytoplankton bloom.
Algal bloom
Algal polysaccharide
Alpha-glucan
Bacterioplankton
Bacteroidota
Beta-glucan
Helgoland Roads LTER
Laminarin
Journal
Microbiome
ISSN: 2049-2618
Titre abrégé: Microbiome
Pays: England
ID NLM: 101615147
Informations de publication
Date de publication:
17 04 2023
17 04 2023
Historique:
received:
18
11
2022
accepted:
15
03
2023
medline:
19
4
2023
entrez:
18
4
2023
pubmed:
19
4
2023
Statut:
epublish
Résumé
Blooms of marine microalgae play a pivotal role in global carbon cycling. Such blooms entail successive blooms of specialized clades of planktonic bacteria that collectively remineralize gigatons of algal biomass on a global scale. This biomass is largely composed of distinct polysaccharides, and the microbial decomposition of these polysaccharides is therefore a process of prime importance. In 2020, we sampled a complete biphasic spring bloom in the German Bight over a 90-day period. Bacterioplankton metagenomes from 30 time points allowed reconstruction of 251 metagenome-assembled genomes (MAGs). Corresponding metatranscriptomes highlighted 50 particularly active MAGs of the most abundant clades, including many polysaccharide degraders. Saccharide measurements together with bacterial polysaccharide utilization loci (PUL) expression data identified β-glucans (diatom laminarin) and α-glucans as the most prominent and actively metabolized dissolved polysaccharide substrates. Both substrates were consumed throughout the bloom, with α-glucan PUL expression peaking at the beginning of the second bloom phase shortly after a peak in flagellate and the nadir in bacterial total cell counts. We show that the amounts and composition of dissolved polysaccharides, in particular abundant storage polysaccharides, have a pronounced influence on the composition of abundant bacterioplankton members during phytoplankton blooms, some of which compete for similar polysaccharide niches. We hypothesize that besides the release of algal glycans, also recycling of bacterial glycans as a result of increased bacterial cell mortality can have a significant influence on bacterioplankton composition during phytoplankton blooms. Video Abstract.
Sections du résumé
BACKGROUND
Blooms of marine microalgae play a pivotal role in global carbon cycling. Such blooms entail successive blooms of specialized clades of planktonic bacteria that collectively remineralize gigatons of algal biomass on a global scale. This biomass is largely composed of distinct polysaccharides, and the microbial decomposition of these polysaccharides is therefore a process of prime importance.
RESULTS
In 2020, we sampled a complete biphasic spring bloom in the German Bight over a 90-day period. Bacterioplankton metagenomes from 30 time points allowed reconstruction of 251 metagenome-assembled genomes (MAGs). Corresponding metatranscriptomes highlighted 50 particularly active MAGs of the most abundant clades, including many polysaccharide degraders. Saccharide measurements together with bacterial polysaccharide utilization loci (PUL) expression data identified β-glucans (diatom laminarin) and α-glucans as the most prominent and actively metabolized dissolved polysaccharide substrates. Both substrates were consumed throughout the bloom, with α-glucan PUL expression peaking at the beginning of the second bloom phase shortly after a peak in flagellate and the nadir in bacterial total cell counts.
CONCLUSIONS
We show that the amounts and composition of dissolved polysaccharides, in particular abundant storage polysaccharides, have a pronounced influence on the composition of abundant bacterioplankton members during phytoplankton blooms, some of which compete for similar polysaccharide niches. We hypothesize that besides the release of algal glycans, also recycling of bacterial glycans as a result of increased bacterial cell mortality can have a significant influence on bacterioplankton composition during phytoplankton blooms. Video Abstract.
Identifiants
pubmed: 37069671
doi: 10.1186/s40168-023-01517-x
pii: 10.1186/s40168-023-01517-x
pmc: PMC10108472
doi:
Substances chimiques
Polysaccharides
0
Types de publication
Video-Audio Media
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
77Informations de copyright
© 2023. The Author(s).
Références
Environ Microbiol. 2007 May;9(5):1253-66
pubmed: 17472638
Front Microbiol. 2021 Apr 01;12:643730
pubmed: 33868201
Bioinformatics. 2012 Dec 15;28(24):3211-7
pubmed: 23071270
Genome Inform. 2009 Oct;23(1):205-11
pubmed: 20180275
Nucleic Acids Res. 2009 Jan;37(Database issue):D233-8
pubmed: 18838391
ISME J. 2021 Mar;15(3):762-773
pubmed: 33097854
Nat Methods. 2012 Mar 04;9(4):357-9
pubmed: 22388286
Nucleic Acids Res. 2016 Jan 4;44(D1):D67-72
pubmed: 26590407
Bioinformatics. 2014 Jul 15;30(14):2068-9
pubmed: 24642063
Oecologia. 1993 Jul;94(4):585-594
pubmed: 28314001
ISME J. 2015 Jun;9(6):1410-22
pubmed: 25478683
Science. 2005 Aug 19;309(5738):1242-5
pubmed: 16109880
ISME J. 2020 Jun;14(6):1369-1383
pubmed: 32071394
ISME J. 2022 Mar;16(3):630-641
pubmed: 34493810
Environ Microbiome. 2021 Aug 17;16(1):15
pubmed: 34404489
PeerJ. 2019 Jul 26;7:e7359
pubmed: 31388474
Nucleic Acids Res. 2004 Feb 25;32(4):1363-71
pubmed: 14985472
Elife. 2016 Apr 07;5:e11888
pubmed: 27054497
Proc Natl Acad Sci U S A. 2018 Mar 27;115(13):E3055-E3064
pubmed: 29531038
Nat Commun. 2021 Feb 19;12(1):1150
pubmed: 33608542
ISME J. 2019 Jan;13(1):76-91
pubmed: 30111868
Environ Microbiol. 2015 Oct;17(10):3515-26
pubmed: 24725270
ISME J. 2019 Nov;13(11):2800-2816
pubmed: 31316134
Environ Microbiol. 2018 Nov;20(11):4127-4140
pubmed: 30246424
Syst Appl Microbiol. 2013 Oct;36(7):497-504
pubmed: 23957959
ISME J. 2017 Dec;11(12):2864-2868
pubmed: 28742071
Appl Environ Microbiol. 2007 Aug;73(16):5261-7
pubmed: 17586664
Environ Microbiol. 2012 Mar;14(3):630-40
pubmed: 21981742
Mar Drugs. 2015 Sep 18;13(9):5993-6018
pubmed: 26393622
Nucleic Acids Res. 2007;35(21):7188-96
pubmed: 17947321
Nat Biotechnol. 2019 May;37(5):540-546
pubmed: 30936562
Nucleic Acids Res. 2013 Jan;41(Database issue):D590-6
pubmed: 23193283
Proc Natl Acad Sci U S A. 2020 Mar 24;117(12):6599-6607
pubmed: 32170018
Syst Appl Microbiol. 2019 Jan;42(1):41-53
pubmed: 30193855
Philos Trans R Soc Lond B Biol Sci. 2017 Sep 5;372(1728):
pubmed: 28717023
Syst Appl Microbiol. 2020 Mar;43(2):126066
pubmed: 32019686
Science. 1998 Jul 10;281(5374):237-40
pubmed: 9657713
Science. 1998 Jul 10;281(5374):200-7
pubmed: 9660741
Syst Appl Microbiol. 2020 Jul;43(4):126088
pubmed: 32690198
Environ Microbiol. 2017 Mar;19(3):1209-1221
pubmed: 28000419
Nucleic Acids Res. 2022 Jan 7;50(D1):D785-D794
pubmed: 34520557
Nucleic Acids Res. 2004 Jan 02;32(1):11-6
pubmed: 14704338
Nucleic Acids Res. 2010 Nov;38(20):e191
pubmed: 20805240
Genome Res. 2015 Jul;25(7):1043-55
pubmed: 25977477
Nat Methods. 2015 Jan;12(1):59-60
pubmed: 25402007
Nucleic Acids Res. 2016 Jan 4;44(D1):D279-85
pubmed: 26673716
Sci Rep. 2021 Nov 3;11(1):21621
pubmed: 34732760
Bioinformatics. 2011 Mar 15;27(6):863-4
pubmed: 21278185
Mikrobiologiia. 2002 Nov-Dec;71(6):725-40
pubmed: 12526193
Nucleic Acids Res. 2000 Jan 1;28(1):27-30
pubmed: 10592173
Science. 2012 May 4;336(6081):608-11
pubmed: 22556258
ISME J. 2018 Dec;12(12):2894-2906
pubmed: 30061707
Bioinformatics. 2019 Nov 15;:
pubmed: 31730192
FEMS Microbiol Ecol. 2017 Mar 1;93(3):
pubmed: 28115400
Front Microbiol. 2019 Jan 24;9:3349
pubmed: 30733714
PeerJ. 2015 Oct 08;3:e1319
pubmed: 26500826
Nat Biotechnol. 2017 Aug 8;35(8):725-731
pubmed: 28787424
Nucleic Acids Res. 2016 Jan 4;44(D1):D286-93
pubmed: 26582926