Bacterial community dynamics during embryonic development of the little skate (Leucoraja erinacea).
Chondrichthyes
Egg capsule
Microbial transmission
Oviparity
Rajidae
Journal
Animal microbiome
ISSN: 2524-4671
Titre abrégé: Anim Microbiome
Pays: England
ID NLM: 101759457
Informations de publication
Date de publication:
13 Oct 2021
13 Oct 2021
Historique:
received:
25
06
2021
accepted:
26
09
2021
entrez:
14
10
2021
pubmed:
15
10
2021
medline:
15
10
2021
Statut:
epublish
Résumé
Microbial transmission from parent to offspring is hypothesized to be widespread in vertebrates. However, evidence for this is limited as many evolutionarily important clades remain unexamined. There is currently no data on the microbiota associated with any Chondrichthyan species during embryonic development, despite the global distribution, ecological importance, and phylogenetic position of this clade. In this study, we take the first steps towards filling this gap by investigating the microbiota associated with embryonic development in the little skate, Leucoraja erinacea, a common North Atlantic species and popular system for chondrichthyan biology. To assess the potential for bacterial transmission in an oviparous chondrichthyan, we used 16S rRNA amplicon sequencing to characterize the microbial communities associated with the skin, gill, and egg capsule of the little skate, at six points during ontogeny. Community composition was analyzed using the QIIME2 pipeline and microbial continuity between stages was tracked using FEAST. We identify site-specific and stage-specific microbiota dominated by the bacterial phyla Proteobacteria and Bacteroidetes. This composition is similar to, but distinct from, that of previously published data on the adult microbiota of other chondrichthyan species. Our data reveal that the skate egg capsule harbors a highly diverse bacterial community-particularly on the internal surface of the capsule-and facilitates intergenerational microbial transfer to the offspring. Embryonic skin and external gill tissues host similar bacterial communities; the skin and gill communities later diverge as the internal gills and skin denticles develop. Our study is the first exploration of the chondrichthyan microbiota throughout ontogeny and provides the first evidence of vertical transmission in this group.
Sections du résumé
BACKGROUND
BACKGROUND
Microbial transmission from parent to offspring is hypothesized to be widespread in vertebrates. However, evidence for this is limited as many evolutionarily important clades remain unexamined. There is currently no data on the microbiota associated with any Chondrichthyan species during embryonic development, despite the global distribution, ecological importance, and phylogenetic position of this clade. In this study, we take the first steps towards filling this gap by investigating the microbiota associated with embryonic development in the little skate, Leucoraja erinacea, a common North Atlantic species and popular system for chondrichthyan biology.
METHODS
METHODS
To assess the potential for bacterial transmission in an oviparous chondrichthyan, we used 16S rRNA amplicon sequencing to characterize the microbial communities associated with the skin, gill, and egg capsule of the little skate, at six points during ontogeny. Community composition was analyzed using the QIIME2 pipeline and microbial continuity between stages was tracked using FEAST.
RESULTS
RESULTS
We identify site-specific and stage-specific microbiota dominated by the bacterial phyla Proteobacteria and Bacteroidetes. This composition is similar to, but distinct from, that of previously published data on the adult microbiota of other chondrichthyan species. Our data reveal that the skate egg capsule harbors a highly diverse bacterial community-particularly on the internal surface of the capsule-and facilitates intergenerational microbial transfer to the offspring. Embryonic skin and external gill tissues host similar bacterial communities; the skin and gill communities later diverge as the internal gills and skin denticles develop.
CONCLUSIONS
CONCLUSIONS
Our study is the first exploration of the chondrichthyan microbiota throughout ontogeny and provides the first evidence of vertical transmission in this group.
Identifiants
pubmed: 34645528
doi: 10.1186/s42523-021-00136-x
pii: 10.1186/s42523-021-00136-x
pmc: PMC8513177
doi:
Types de publication
Journal Article
Langues
eng
Pagination
72Subventions
Organisme : national science foundation
ID : DGE1745303
Organisme : Microbiome Center of the University of Chicago, Marine Biological Laboratory, and Argonne National Laboratory
ID : Microbiome Pilot Project Grant
Informations de copyright
© 2021. The Author(s).
Références
PLoS One. 2011;6(7):e22339
pubmed: 21811590
Proc Biol Sci. 2020 Sep 9;287(1934):20200820
pubmed: 32873208
Nat Methods. 2019 Jul;16(7):627-632
pubmed: 31182859
Sci Adv. 2018 Nov 07;4(11):eaau5484
pubmed: 30417097
FEMS Microbiol Ecol. 2013 Sep;85(3):483-94
pubmed: 23607777
PLoS One. 2020 May 5;15(5):e0232698
pubmed: 32369496
Naturwissenschaften. 2011 Nov;98(11):951-60
pubmed: 21964973
BMC Bioinformatics. 2014 Feb 05;15:41
pubmed: 24499292
Front Biosci (Landmark Ed). 2010 Jan 01;15:25-34
pubmed: 20036803
Front Microbiol. 2021 Feb 11;12:605285
pubmed: 33643235
F1000Res. 2016 Jun 24;5:1492
pubmed: 27508062
Environ Microbiol Rep. 2017 Aug;9(4):357-373
pubmed: 28418094
Nucleic Acids Res. 2014 Jan;42(Database issue):D643-8
pubmed: 24293649
PLoS One. 2014 Mar 26;9(3):e90785
pubmed: 24671052
Int J Syst Evol Microbiol. 2016 Sep;66(9):3625-3631
pubmed: 27307140
Nat Methods. 2016 Jul;13(7):581-3
pubmed: 27214047
Environ Microbiol. 2017 Apr;19(4):1463-1475
pubmed: 28063183
Experientia. 1978 Dec 15;34(12):1596-7
pubmed: 569596
PLoS One. 2013 Apr 22;8(4):e61217
pubmed: 23630581
mBio. 2019 Oct 8;10(5):
pubmed: 31594812
Microbiome. 2017 Mar 3;5(1):27
pubmed: 28253908
Environ Microbiol. 2001 Mar;3(3):151-67
pubmed: 11321532
F1000Res. 2014 Aug 12;3:191
pubmed: 25309735
Int J Syst Evol Microbiol. 2017 Dec;67(12):5067-5079
pubmed: 29034851
ISME J. 2014 Dec;8(12):2431-44
pubmed: 25036926
Zoo Biol. 2017 May;36(3):226-230
pubmed: 28544080
Sci Rep. 2017 Nov 10;7(1):15269
pubmed: 29127421
J Morphol. 2017 Mar;278(3):300-320
pubmed: 28144984
Anat Rec (Hoboken). 2008 Sep;291(9):1079-87
pubmed: 18493933
J Fish Biol. 2012 Apr;80(5):1141-58
pubmed: 22497376
Antimicrob Resist Infect Control. 2014 Sep 17;3:28
pubmed: 25232470
PLoS Biol. 2013;11(8):e1001631
pubmed: 23976878
Anim Microbiome. 2019 Sep 17;1(1):9
pubmed: 33499949
Peptides. 2005 Apr;26(4):581-7
pubmed: 15752571
Mol Phylogenet Evol. 2014 Jun;75:245-51
pubmed: 24486989
FEMS Microbiol Ecol. 2015 Jul;91(7):
pubmed: 26048284
J Endourol. 2011 Sep;25(9):1547-52
pubmed: 21819223
Front Microbiol. 2012 Aug 23;3:292
pubmed: 22936927
Mar Pollut Bull. 2019 Aug;145:595-603
pubmed: 31590829
Comp Biochem Physiol B Biochem Mol Biol. 2003 Dec;136(4):685-700
pubmed: 14662294
Proc Natl Acad Sci U S A. 2015 Dec 29;112(52):15940-5
pubmed: 26644578
Microbiome. 2020 Jun 13;8(1):93
pubmed: 32534596
Proc Biol Sci. 2019 Nov 6;286(1914):20191571
pubmed: 31662089
Genome Biol. 2011 Jun 24;12(6):R60
pubmed: 21702898
J Anim Ecol. 2020 Jul;89(7):1549-1558
pubmed: 32248522
Front Microbiol. 2017 Jul 05;8:1050
pubmed: 28725216
J Fish Biol. 2012 Apr;80(5):1940-67
pubmed: 22497413
PLoS One. 2014 Apr 10;9(4):e94249
pubmed: 24722003
Microbiome. 2018 May 17;6(1):90
pubmed: 29773078
ISME J. 2013 May;7(5):1026-37
pubmed: 23303374
Proc Biol Sci. 2020 Mar 11;287(1922):20192900
pubmed: 32126958
Appl Environ Microbiol. 2018 Apr 16;84(9):
pubmed: 29453266
Elife. 2020 May 12;9:
pubmed: 32393435
Data Brief. 2018 Oct 24;21:1029-1032
pubmed: 30450395
Nat Biotechnol. 2019 Aug;37(8):852-857
pubmed: 31341288
Microbiologyopen. 2019 Apr;8(4):e00672
pubmed: 29897674
Int J Syst Evol Microbiol. 2019 Oct;69(10):3148-3154
pubmed: 31385778