Unveiling microbiome changes in Mediterranean octocorals during the 2022 marine heatwaves: quantifying key bacterial symbionts and potential pathogens.
16S rRNA gene sequencing
Bacterial communities
Climate change
Corallium rubrum
Endozoicomonas
Gene expression
Holobiont
Marine heatwaves
Paramuricea clavata
Spirochaetaceae
qPCR
Journal
Microbiome
ISSN: 2049-2618
Titre abrégé: Microbiome
Pays: England
ID NLM: 101615147
Informations de publication
Date de publication:
05 Dec 2023
05 Dec 2023
Historique:
received:
21
07
2023
accepted:
27
10
2023
medline:
7
12
2023
pubmed:
6
12
2023
entrez:
5
12
2023
Statut:
epublish
Résumé
Climate change has accelerated the occurrence and severity of heatwaves in the Mediterranean Sea and poses a significant threat to the octocoral species that form the foundation of marine animal forests (MAFs). As coral health intricately relies on the symbiotic relationships established between corals and microbial communities, our goal was to gain a deeper understanding of the role of bacteria in the observed tissue loss of key octocoral species following the unprecedented heatwaves in 2022. Using amplicon sequencing and taxon-specific qPCR analyses, we unexpectedly found that the absolute abundance of the major bacterial symbionts, Spirochaetaceae (C. rubrum) and Endozoicomonas (P. clavata), remained, in most cases, unchanged between colonies with 0% and 90% tissue loss. These results suggest that the impairment of coral health was not due to the loss of the main bacterial symbionts. However, we observed a significant increase in the total abundance of bacterial opportunists, including putative pathogens such as Vibrio, which was not evident when only their relative abundance was considered. In addition, there was no clear relation between bacterial symbiont loss and the intensity of thermal stress, suggesting that factors other than temperature may have influenced the differential response of octocoral microbiomes at different sampling sites. Our results indicate that tissue loss in octocorals is not directly caused by the decline of the main bacterial symbionts but by the proliferation of opportunistic and pathogenic bacteria. Our findings thus underscore the significance of considering both relative and absolute quantification approaches when evaluating the impact of stressors on coral microbiome as the relative quantification does not accurately depict the actual changes in the microbiome. Consequently, this research enhances our comprehension of the intricate interplay between host organisms, their microbiomes, and environmental stressors, while offering valuable insights into the ecological implications of heatwaves on marine animal forests. Video Abstract.
Sections du résumé
BACKGROUND
BACKGROUND
Climate change has accelerated the occurrence and severity of heatwaves in the Mediterranean Sea and poses a significant threat to the octocoral species that form the foundation of marine animal forests (MAFs). As coral health intricately relies on the symbiotic relationships established between corals and microbial communities, our goal was to gain a deeper understanding of the role of bacteria in the observed tissue loss of key octocoral species following the unprecedented heatwaves in 2022.
RESULTS
RESULTS
Using amplicon sequencing and taxon-specific qPCR analyses, we unexpectedly found that the absolute abundance of the major bacterial symbionts, Spirochaetaceae (C. rubrum) and Endozoicomonas (P. clavata), remained, in most cases, unchanged between colonies with 0% and 90% tissue loss. These results suggest that the impairment of coral health was not due to the loss of the main bacterial symbionts. However, we observed a significant increase in the total abundance of bacterial opportunists, including putative pathogens such as Vibrio, which was not evident when only their relative abundance was considered. In addition, there was no clear relation between bacterial symbiont loss and the intensity of thermal stress, suggesting that factors other than temperature may have influenced the differential response of octocoral microbiomes at different sampling sites.
CONCLUSIONS
CONCLUSIONS
Our results indicate that tissue loss in octocorals is not directly caused by the decline of the main bacterial symbionts but by the proliferation of opportunistic and pathogenic bacteria. Our findings thus underscore the significance of considering both relative and absolute quantification approaches when evaluating the impact of stressors on coral microbiome as the relative quantification does not accurately depict the actual changes in the microbiome. Consequently, this research enhances our comprehension of the intricate interplay between host organisms, their microbiomes, and environmental stressors, while offering valuable insights into the ecological implications of heatwaves on marine animal forests. Video Abstract.
Identifiants
pubmed: 38053218
doi: 10.1186/s40168-023-01711-x
pii: 10.1186/s40168-023-01711-x
pmc: PMC10696765
doi:
Types de publication
Video-Audio Media
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
271Informations de copyright
© 2023. The Author(s).
Références
Front Microbiol. 2023 Feb 03;14:1116737
pubmed: 36819038
Microorganisms. 2021 Oct 20;9(11):
pubmed: 34835306
Front Microbiol. 2017 Nov 15;8:2224
pubmed: 29187837
Proc Biol Sci. 2023 Jun 14;290(2000):20222539
pubmed: 37282536
Front Microbiol. 2019 Sep 24;10:2244
pubmed: 31608047
Sci Total Environ. 2022 Jun 1;823:153701
pubmed: 35134420
Appl Environ Microbiol. 2008 Jan;74(1):52-60
pubmed: 17965206
ISME J. 2022 Aug;16(8):1883-1895
pubmed: 35444262
Integr Comp Biol. 2010 Oct;50(4):662-74
pubmed: 21558231
Glob Chang Biol. 2023 Apr;29(7):1681-1683
pubmed: 36660905
Mol Syst Biol. 2011 Oct 11;7:539
pubmed: 21988835
Front Microbiol. 2017 Mar 07;8:341
pubmed: 28326066
Mol Ecol. 2021 Sep;30(18):4466-4480
pubmed: 34342082
Nat Methods. 2016 Jul;13(7):581-3
pubmed: 27214047
Mar Pollut Bull. 2018 Jun;131(Pt A):87-94
pubmed: 29887008
PLoS One. 2013 Apr 22;8(4):e61217
pubmed: 23630581
Mar Environ Res. 2011 Jul;72(1-2):67-74
pubmed: 21700328
Nat Commun. 2020 Jul 14;11(1):3514
pubmed: 32665548
Glob Chang Biol. 2023 Nov;29(22):6159-6162
pubmed: 37681400
ISME Commun. 2023 Mar 9;3(1):19
pubmed: 36894742
Appl Environ Microbiol. 2009 Jun;75(11):3492-501
pubmed: 19346350
Nat Rev Microbiol. 2014 Oct;12(10):686-98
pubmed: 25134618
Appl Environ Microbiol. 2012 May;78(9):3136-44
pubmed: 22344646
FEMS Microbiol Lett. 2009 Mar;292(2):210-5
pubmed: 19191871
Front Cell Infect Microbiol. 2020 Aug 07;10:403
pubmed: 32850498
Sci Rep. 2016 Jun 06;6:27277
pubmed: 27263657
Microb Ecol. 2012 Apr;63(3):605-18
pubmed: 21984347
PLoS One. 2013 Apr 22;8(4):e62091
pubmed: 23630625
Environ Microbiol. 2010 Jul;12(7):2007-19
pubmed: 20370818
Front Microbiol. 2020 Apr 23;11:681
pubmed: 32425901
Front Microbiol. 2015 May 18;6:432
pubmed: 26042096
PLoS One. 2011;6(9):e23814
pubmed: 21931615
Coral Reefs. 2023;42(1):131-142
pubmed: 36415309
Science. 2006 Nov 3;314(5800):787-90
pubmed: 17082450
Microb Ecol. 2018 Jan;75(1):274-288
pubmed: 28681143
Nucleic Acids Res. 2001 May 1;29(9):e45
pubmed: 11328886
FEMS Microbiol Ecol. 2014 Nov;90(2):404-16
pubmed: 25078065
J Environ Manage. 2022 Jan 1;301:113919
pubmed: 34731944
Annu Rev Microbiol. 2016 Sep 8;70:317-40
pubmed: 27482741
Appl Environ Microbiol. 2005 Jul;71(7):4117-20
pubmed: 16000830
Microb Ecol. 2017 Feb;73(2):466-478
pubmed: 27726033
J Infect Dis. 2021 Jun 16;223(12 Suppl 2):S270-S275
pubmed: 33330938
Nat Commun. 2018 Apr 10;9(1):1324
pubmed: 29636482
Appl Environ Microbiol. 2022 Mar 22;88(6):e0234021
pubmed: 35108095
Appl Environ Microbiol. 2004 Jul;70(7):4103-10
pubmed: 15240289
Environ Microbiome. 2023 Aug 14;18(1):70
pubmed: 37580830
Bioinformatics. 2018 Aug 15;34(16):2870-2878
pubmed: 29608657
Glob Chang Biol. 2022 Oct;28(19):5708-5725
pubmed: 35848527
PLoS Comput Biol. 2014 Apr 03;10(4):e1003531
pubmed: 24699258
Science. 2002 Feb 15;295(5558):1280-4
pubmed: 11847338
Front Microbiol. 2020 Jul 31;11:1791
pubmed: 32849407
Front Microbiol. 2019 Oct 23;10:2407
pubmed: 31708888
Microbiologyopen. 2017 Aug;6(4):
pubmed: 28425179
Water Res. 2002 Feb;36(3):779-82
pubmed: 11827339
Sci Rep. 2019 Apr 11;9(1):5911
pubmed: 30976028
Environ Microbiol. 2020 May;22(5):1675-1687
pubmed: 31943674