Biphasic cellular adaptations and ecological implications of Alteromonas macleodii degrading a mixture of algal polysaccharides.
Journal
The ISME journal
ISSN: 1751-7370
Titre abrégé: ISME J
Pays: England
ID NLM: 101301086
Informations de publication
Date de publication:
01 2019
01 2019
Historique:
received:
09
05
2018
accepted:
19
07
2018
revised:
10
07
2018
pubmed:
18
8
2018
medline:
1
8
2019
entrez:
18
8
2018
Statut:
ppublish
Résumé
Algal polysaccharides are an important bacterial nutrient source and central component of marine food webs. However, cellular and ecological aspects concerning the bacterial degradation of polysaccharide mixtures, as presumably abundant in natural habitats, are poorly understood. Here, we contextualize marine polysaccharide mixtures and their bacterial utilization in several ways using the model bacterium Alteromonas macleodii 83-1, which can degrade multiple algal polysaccharides and contributes to polysaccharide degradation in the oceans. Transcriptomic, proteomic and exometabolomic profiling revealed cellular adaptations of A. macleodii 83-1 when degrading a mix of laminarin, alginate and pectin. Strain 83-1 exhibited substrate prioritization driven by catabolite repression, with initial laminarin utilization followed by simultaneous alginate/pectin utilization. This biphasic phenotype coincided with pronounced shifts in gene expression, protein abundance and metabolite secretion, mainly involving CAZymes/polysaccharide utilization loci but also other functional traits. Distinct temporal changes in exometabolome composition, including the alginate/pectin-specific secretion of pyrroloquinoline quinone, suggest that substrate-dependent adaptations influence chemical interactions within the community. The ecological relevance of cellular adaptations was underlined by molecular evidence that common marine macroalgae, in particular Saccharina and Fucus, release mixtures of alginate and pectin-like rhamnogalacturonan. Moreover, CAZyme microdiversity and the genomic predisposition towards polysaccharide mixtures among Alteromonas spp. suggest polysaccharide-related traits as an ecophysiological factor, potentially relating to distinct 'carbohydrate utilization types' with different ecological strategies. Considering the substantial primary productivity of algae on global scales, these insights contribute to the understanding of bacteria-algae interactions and the remineralization of chemically diverse polysaccharide pools, a key step in marine carbon cycling.
Identifiants
pubmed: 30116038
doi: 10.1038/s41396-018-0252-4
pii: 10.1038/s41396-018-0252-4
pmc: PMC6298977
doi:
Substances chimiques
Alginates
0
Polysaccharides
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Pagination
92-103Références
Sci Rep. 2012;2:696
pubmed: 23019517
Environ Microbiol. 2017 Jun;19(6):2320-2333
pubmed: 28276126
Mol Microbiol. 2017 Apr;104(1):32-45
pubmed: 28009067
Water Res. 2015 Apr 15;73:216-30
pubmed: 25682049
Environ Microbiol. 2016 Dec;18(12):4456-4470
pubmed: 27348854
PLoS One. 2011 Feb 03;6(2):e16805
pubmed: 21304826
Proc Natl Acad Sci U S A. 2016 May 31;113(22):6188-93
pubmed: 27185956
ISME J. 2015 Jun;9(6):1410-22
pubmed: 25478683
Nucleic Acids Res. 2016 Jan 4;44(D1):D447-56
pubmed: 26527722
PLoS One. 2016 Mar 10;11(3):e0150820
pubmed: 26963515
ISME J. 2008 Dec;2(12):1194-212
pubmed: 18670397
Environ Microbiol. 2012 Aug;14(8):1898-912
pubmed: 22222000
J Proteome Res. 2006 Sep;5(9):2339-47
pubmed: 16944946
Nucleic Acids Res. 2017 Jan 4;45(D1):D190-D199
pubmed: 27899635
Mol Microbiol. 2012 Aug;85(3):478-91
pubmed: 22686399
Environ Microbiol Rep. 2017 Apr;9(2):151-157
pubmed: 27943607
Mol Biosyst. 2010 Dec;6(12):2363-72
pubmed: 20938502
Sci Data. 2016 Jul 05;3:160050
pubmed: 27377622
Environ Microbiol. 2016 Dec;18(12):4610-4627
pubmed: 27768819
J Ind Microbiol Biotechnol. 1999 Aug;23(2):123-126
pubmed: 10510491
Elife. 2016 Apr 07;5:e11888
pubmed: 27054497
Genome Biol. 2014;15(12):550
pubmed: 25516281
Microbiology (Reading). 1994 Sep;140 ( Pt 9):2451-8
pubmed: 7952195
Nat Rev Microbiol. 2008 Aug;6(8):613-24
pubmed: 18628769
Acta Crystallogr D Biol Crystallogr. 2015 Feb;71(Pt 2):173-84
pubmed: 25664729
Proteomics. 2009 Jul;9(14):3677-97
pubmed: 19639587
J Bacteriol. 2017 Jul 11;199(15):
pubmed: 28138099
Science. 1992 Mar 20;255(5051):1561-4
pubmed: 17820170
ISME J. 2017 Jul;11(7):1640-1650
pubmed: 28323277
Environ Microbiol. 2015 Oct;17(10):3857-68
pubmed: 25847866
Environ Microbiol. 2007 Jun;9(6):1415-22
pubmed: 17504479
Sci Rep. 2016 Nov 30;6:38248
pubmed: 27901120
Mol Microbiol. 2013 Jun;88(5):876-90
pubmed: 23646867
Nat Microbiol. 2017 Nov;2(11):1533-1542
pubmed: 28894102
Environ Microbiol. 2012 Sep;14(9):2379-94
pubmed: 22513138
Environ Microbiol. 2017 Jun;19(6):2164-2181
pubmed: 28205313
Front Microbiol. 2015 May 27;6:523
pubmed: 26074905
ISME J. 2018 Apr;12(4):981-996
pubmed: 29335641
Nucleic Acids Res. 2017 Jan 4;45(D1):D507-D516
pubmed: 27738135
Biochim Biophys Acta. 2000 Dec 29;1543(2):361-382
pubmed: 11150614
Curr Opin Struct Biol. 2014 Oct;28:77-86
pubmed: 25136767
ISME J. 2018 Dec;12(12):2823-2834
pubmed: 30022156
Front Microbiol. 2017 Sep 21;8:1808
pubmed: 28983288
Microb Genom. 2016 Feb 9;2(2):e000043
pubmed: 28348841
Nucleic Acids Res. 2015 Jul 1;43(W1):W30-8
pubmed: 25943547
Environ Microbiol. 2016 Dec;18(12):4369-4377
pubmed: 27059936
Nat Commun. 2016 Sep 22;7:12860
pubmed: 27653556
Sci Rep. 2016 Apr 13;6:24373
pubmed: 27071527
mBio. 2017 Oct 10;8(5):
pubmed: 29018117
Mar Biotechnol (NY). 2016 Feb;18(1):15-23
pubmed: 26458373
J Biol Chem. 2014 Jan 24;289(4):2027-42
pubmed: 24337571
PLoS One. 2012;7(4):e35314
pubmed: 22536372
ISME J. 2017 Aug;11(8):1813-1824
pubmed: 28440800
J Phycol. 2015 Oct;51(5):885-95
pubmed: 26986885
Mol Ecol. 2008 Sep;17(18):4092-106
pubmed: 19238708
J Biol Chem. 2015 Apr 3;290(14):9020-36
pubmed: 25657012
Water Res. 2003 Nov;37(18):4311-30
pubmed: 14511701
Nucleic Acids Res. 2016 Jan 4;44(D1):D372-9
pubmed: 26546518
Front Microbiol. 2017 Feb 14;8:220
pubmed: 28261179
Appl Environ Microbiol. 2017 Apr 17;83(9):
pubmed: 28213541
ISME J. 2013 Jun;7(6):1187-99
pubmed: 23303371
Front Microbiol. 2014 Jun 03;5:267
pubmed: 24917860
Mol Biol Evol. 2013 May;30(5):1218-23
pubmed: 23412913
Genome Biol Evol. 2013;5(6):1220-32
pubmed: 23729633
Nat Commun. 2017 Nov 22;8(1):1685
pubmed: 29162826
Nucleic Acids Res. 2012 Jul;40(Web Server issue):W445-51
pubmed: 22645317
FEMS Microbiol Lett. 1998 Feb 15;159(2):261-6
pubmed: 9503620
ISME J. 2016 Dec;10(12):2892-2906
pubmed: 27128996
ISME J. 2014 Jul;8(7):1492-502
pubmed: 24522261
ISME J. 2013 May;7(5):1026-37
pubmed: 23303374
Nature. 2015 Jan 8;517(7533):165-169
pubmed: 25567280
Microb Ecol. 2007 May;53(4):513-23
pubmed: 17333428
Front Microbiol. 2017 Jan 31;8:65
pubmed: 28197132
Biochem J. 1961 Jun;79:531-7
pubmed: 13688276
PLoS Genet. 2008 May 30;4(5):e1000087
pubmed: 18516288
Microbiologyopen. 2017 Feb;6(1):
pubmed: 27987272
PLoS One. 2011;6(12):e28900
pubmed: 22216139
Science. 2012 May 4;336(6081):608-11
pubmed: 22556258
Environ Microbiol. 2015 Oct;17(10):3822-31
pubmed: 25753990
Front Microbiol. 2016 Jun 09;7:880
pubmed: 27375600
Nat Commun. 2015 Sep 22;6:8289
pubmed: 26392107
Bioinformatics. 2014 Jul 15;30(14):2068-9
pubmed: 24642063
Microbes Environ. 2015;30(2):123-5
pubmed: 26094633
Nucleic Acids Res. 2004 Mar 19;32(5):1792-7
pubmed: 15034147
Mol Biol Evol. 2009 Jul;26(7):1641-50
pubmed: 19377059
Syst Appl Microbiol. 2013 Feb;36(1):39-48
pubmed: 23265193
mSystems. 2017 Nov 14;2(6):
pubmed: 29152587
Nucleic Acids Res. 2014 Jul;42(Web Server issue):W320-4
pubmed: 24753421
ISME J. 2013 May;7(5):962-79
pubmed: 23303369
Appl Microbiol Biotechnol. 2014 May;98(10):4545-55
pubmed: 24463762
Nucleic Acids Res. 2014 Jan;42(Database issue):D490-5
pubmed: 24270786