Mono-specific algal diets shape microbial networking in the gut of the sea urchin Tripneustes gratilla elatensis.
Journal
Animal microbiome
ISSN: 2524-4671
Titre abrégé: Anim Microbiome
Pays: England
ID NLM: 101759457
Informations de publication
Date de publication:
15 Nov 2021
15 Nov 2021
Historique:
received:
21
04
2021
accepted:
15
10
2021
entrez:
16
11
2021
pubmed:
17
11
2021
medline:
17
11
2021
Statut:
epublish
Résumé
Algivorous sea urchins can obtain energy from a diet of a single algal species, which may result in consequent changes in their gut microbe assemblies and association networks. To ascertain whether such changes are led by specific microbes or limited to a specific region in the gut, we compared the microbial assembly in the three major gut regions of the sea urchin Tripneustes gratilla elatensis when fed a mono-specific algal diet of either Ulva fasciata or Gracilaria conferta, or an algal-free diet. DNA extracts from 5 to 7 individuals from each diet treatment were used for Illumina MiSeq based 16S rRNA gene sequencing (V3-V4 region). Niche breadth of each microbe in the assembly was calculated for identification of core, generalist, specialist, or unique microbes. Network analyzers were used to measure the connectivity of the entire assembly and of each of the microbes within it and whether it altered with a given diet or gut region. Lastly, the predicted metabolic functions of key microbes in the gut were analyzed to evaluate their potential contribution to decomposition of dietary algal polysaccharides. Sea urchins fed with U. fasciata grew faster and their gut microbiome network was rich in bacterial associations (edges) and networking clusters. Bacteroidetes was the keystone microbe phylum in the gut, with core, generalist, and specialist representatives. A few microbes of this phylum were central hub nodes that maintained community connectivity, while others were driver microbes that led the rewiring of the assembly network based on diet type through changes in their associations and centrality. Niche breadth agreed with microbes' richness in genes for carbohydrate active enzymes and correlated Bacteroidetes specialists to decomposition of specific polysaccharides in the algal diets. The dense and well-connected microbial network in the gut of Ulva-fed sea urchins, together with animal's rapid growth, may suggest that this alga was most nutritious among the experimental diets. Our findings expand the knowledge on the gut microbial assembly in T. gratilla elatensis and strengthen the correlation between microbes' generalism or specialism in terms of occurrence in different niches and their metabolic arsenal which may aid host nutrition.
Sections du résumé
BACKGROUND
BACKGROUND
Algivorous sea urchins can obtain energy from a diet of a single algal species, which may result in consequent changes in their gut microbe assemblies and association networks.
METHODS
METHODS
To ascertain whether such changes are led by specific microbes or limited to a specific region in the gut, we compared the microbial assembly in the three major gut regions of the sea urchin Tripneustes gratilla elatensis when fed a mono-specific algal diet of either Ulva fasciata or Gracilaria conferta, or an algal-free diet. DNA extracts from 5 to 7 individuals from each diet treatment were used for Illumina MiSeq based 16S rRNA gene sequencing (V3-V4 region). Niche breadth of each microbe in the assembly was calculated for identification of core, generalist, specialist, or unique microbes. Network analyzers were used to measure the connectivity of the entire assembly and of each of the microbes within it and whether it altered with a given diet or gut region. Lastly, the predicted metabolic functions of key microbes in the gut were analyzed to evaluate their potential contribution to decomposition of dietary algal polysaccharides.
RESULTS
RESULTS
Sea urchins fed with U. fasciata grew faster and their gut microbiome network was rich in bacterial associations (edges) and networking clusters. Bacteroidetes was the keystone microbe phylum in the gut, with core, generalist, and specialist representatives. A few microbes of this phylum were central hub nodes that maintained community connectivity, while others were driver microbes that led the rewiring of the assembly network based on diet type through changes in their associations and centrality. Niche breadth agreed with microbes' richness in genes for carbohydrate active enzymes and correlated Bacteroidetes specialists to decomposition of specific polysaccharides in the algal diets.
CONCLUSIONS
CONCLUSIONS
The dense and well-connected microbial network in the gut of Ulva-fed sea urchins, together with animal's rapid growth, may suggest that this alga was most nutritious among the experimental diets. Our findings expand the knowledge on the gut microbial assembly in T. gratilla elatensis and strengthen the correlation between microbes' generalism or specialism in terms of occurrence in different niches and their metabolic arsenal which may aid host nutrition.
Identifiants
pubmed: 34782025
doi: 10.1186/s42523-021-00140-1
pii: 10.1186/s42523-021-00140-1
pmc: PMC8594234
doi:
Types de publication
Journal Article
Langues
eng
Pagination
79Subventions
Organisme : Israel Ministry of Energy
ID : 215-11-032
Informations de copyright
© 2021. The Author(s).
Références
Microorganisms. 2019 Jan 26;7(2):
pubmed: 30691133
FEMS Microbiol Ecol. 2020 Dec 30;97(1):
pubmed: 33238305
Bioinformatics. 2010 Oct 1;26(19):2460-1
pubmed: 20709691
Environ Microbiol. 2012 Jan;14(1):4-12
pubmed: 22004523
Science. 1999 Oct 15;286(5439):509-12
pubmed: 10521342
FEMS Microbiol Rev. 2013 May;37(3):462-76
pubmed: 23157386
Conserv Physiol. 2014 Mar 21;2(1):cou009
pubmed: 27293630
Microbiologyopen. 2017 Feb;6(1):
pubmed: 27987272
J Biotechnol. 2001 Jul 26;89(1):81-4
pubmed: 11472802
Front Microbiol. 2011 May 30;2:93
pubmed: 21747801
Mar Drugs. 2010 Jan 26;8(1):200-18
pubmed: 20161978
Front Microbiol. 2014 May 20;5:219
pubmed: 24904535
Food Microbiol. 2018 Aug;73:49-60
pubmed: 29526226
Appl Environ Microbiol. 2004 Oct;70(10):6166-72
pubmed: 15466563
FEMS Microbiol Ecol. 2016 Sep;92(9):
pubmed: 27368709
Proc Natl Acad Sci U S A. 2015 May 19;112(20):6449-54
pubmed: 25941371
Trends Microbiol. 2017 Mar;25(3):217-228
pubmed: 27916383
Nat Rev Genet. 2013 Oct;14(10):719-32
pubmed: 24045689
FEMS Microbiol Rev. 2019 Jul 1;43(4):362-379
pubmed: 31050730
Nat Chem Biol. 2019 Aug;15(8):803-812
pubmed: 31285597
Nat Ecol Evol. 2018 Jun;2(6):936-943
pubmed: 29662222
ISME J. 2012 Aug;6(8):1621-4
pubmed: 22402401
Nat Commun. 2017 Oct 27;8(1):1162
pubmed: 29079803
Microbiome. 2020 Jun 4;8(1):82
pubmed: 32498714
PLoS One. 2015 Nov 16;10(11):e0143111
pubmed: 26571275
Front Microbiol. 2019 May 28;10:1168
pubmed: 31191489
Nucleic Acids Res. 2013 Jan;41(Database issue):D590-6
pubmed: 23193283
Front Microbiol. 2012 Dec 19;3:417
pubmed: 23267351
Nat Microbiol. 2019 Dec;4(12):2456-2465
pubmed: 31548685
ISME J. 2015 Jul;9(7):1488-95
pubmed: 25526370
Int J Syst Evol Microbiol. 2011 Dec;61(Pt 12):2885-2889
pubmed: 21257687
Genome Res. 2003 Nov;13(11):2498-504
pubmed: 14597658
mSystems. 2019 Jun 11;4(3):
pubmed: 31186307
Microb Ecol. 1993 May;25(3):195-231
pubmed: 24189919
mSystems. 2015 Dec 22;1(1):
pubmed: 27822518
ISME J. 2019 Feb;13(2):442-454
pubmed: 30287886
FEMS Microbiol Ecol. 2016 Nov;92(11):
pubmed: 27543321
Bioinformatics. 2014 Mar 1;30(5):614-20
pubmed: 24142950
Biol Bull. 1970 Jun;138(3):286-305
pubmed: 5433301
BMC Biol. 2008 Jul 23;6:33
pubmed: 18651948
Nucleic Acids Res. 2020 Jul 2;48(W1):W572-W579
pubmed: 32338757
Genome Biol. 2011 Jun 24;12(6):R60
pubmed: 21702898
Bioinformatics. 2010 Jan 15;26(2):266-7
pubmed: 19914921
J Anim Ecol. 2020 Jul;89(7):1549-1558
pubmed: 32248522
PLoS One. 2013 Oct 23;8(10):e76376
pubmed: 24194836
Nat Protoc. 2020 Mar;15(3):799-821
pubmed: 31942082
Nat Methods. 2010 May;7(5):335-6
pubmed: 20383131
Microb Ecol. 2011 Jan;61(1):20-30
pubmed: 20424834
Appl Environ Microbiol. 2015 Mar;81(6):2090-7
pubmed: 25576616
Nat Rev Microbiol. 2018 Sep;16(9):567-576
pubmed: 29789680
Nucleic Acids Res. 2008 Jul 1;36(Web Server issue):W5-9
pubmed: 18440982
Biomacromolecules. 2007 Jun;8(6):1765-74
pubmed: 17458931
Nucleic Acids Res. 2017 Jul 3;45(W1):W180-W188
pubmed: 28449106
Bioinformatics. 2015 Oct 1;31(19):3172-80
pubmed: 26048598
Nature. 2001 Mar 8;410(6825):268-76
pubmed: 11258382
Front Microbiol. 2015 Oct 13;6:1047
pubmed: 26528245
Front Microbiol. 2019 Apr 24;10:849
pubmed: 31105660
FEMS Microbiol Ecol. 2013 Jan;83(1):1-16
pubmed: 22775757
Front Microbiol. 2020 Feb 28;11:308
pubmed: 32184772
Nucleic Acids Res. 2018 Jul 2;46(W1):W95-W101
pubmed: 29771380
Bioinformatics. 2011 Aug 15;27(16):2194-200
pubmed: 21700674