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Evidence of vent-adaptation in sponges living at the periphery of hydrothermal vent environments: Ecological and evolutionary implications

Evidence of vent-adaptation in sponges living at the periphery of hydrothermal vent environments: Ecological and evolutionary implications
Evidence of vent-adaptation in sponges living at the periphery of hydrothermal vent environments: Ecological and evolutionary implications
The peripheral areas of deep-sea hydrothermal vents are often inhabited by an assemblage of animals distinct to those living close to vent chimneys. For many such taxa, it is considered that peak abundances in the vent periphery relate to the availability of hard substrate as well as the increased concentrations of organic matter generated at vents, compared to background areas. However, the peripheries of vents are less well-studied than the assemblages of vent-endemic taxa, and the mechanisms through which peripheral fauna may benefit from vent environments are generally unknown. Understanding this is crucial for evaluating the sphere of influence of hydrothermal vents and managing the impacts of future human activity within these environments, as well as offering insights into the processes of metazoan adaptation to vents. In this study, we explored the evolutionary histories, microbiomes and nutritional sources of two distantly-related sponge types living at the periphery of active hydrothermal vents in two different geological settings (Cladorhiza from the E2 vent site on the East Scotia Ridge, Southern Ocean, and Spinularia from the Endeavour vent site on the Juan de Fuca Ridge, North-East Pacific) to examine their relationship to nearby venting. Our results uncovered a close sister relationship between the majority of our E2 Cladorhiza specimens and the species Cladorhiza methanophila, known to harbor and obtain nutrition from methanotrophic symbionts at cold seeps. Our microbiome analyses demonstrated that both E2 Cladorhiza and Endeavour Spinularia sp. are associated with putative chemosynthetic Gammaproteobacteria, including Thioglobaceae (present in both sponge types) and Methylomonaceae (present in Spinularia sp.). These bacteria are closely related to chemoautotrophic symbionts of bathymodiolin mussels. Both vent-peripheral sponges demonstrate carbon and nitrogen isotopic signatures consistent with contributions to nutrition from chemosynthesis. This study expands the number of known associations between metazoans and potentially chemosynthetic Gammaproteobacteria, indicating that they can be incredibly widespread and also occur away from the immediate vicinity of chemosynthetic environments in the vent-periphery, where these sponges may be adapted to benefit from dispersed vent fluids.
16S rRNA amplicon, Porifera, chemosynthesis, cold seep, microbiome, nutrition
1664-302X
Georgieva, Magdalena
9e336902-08e7-4ff5-b06b-fc57c0e078d2
Taboada, Sergi
a064593b-c411-473a-ae9f-6c753ded9010
Riesgo, Ana
3e375d1f-2e40-4d69-8c11-20aaf6872bb2
Diez-Vives, Cristina
92c0ec1b-be26-48cf-abe5-4c2d6eaee6d8
De Leo, Fabio
47fce20b-71a6-440e-83fc-333cbc75cbcf
Jeffreys, Rachel
81eebb35-6ff9-4903-a2b1-39a5a3104a84
Copley, Jonathan
5f30e2a6-76c1-4150-9a42-dcfb8f5788ef
Little, Crispin
2f877300-3a98-465c-a033-ab3ac231755d
Rios, Pilar
cf976de9-bc7b-4e21-b146-89a51458fe9b
Cristobo, Javier
6eeae36a-1f42-430d-9600-995da88370d9
Hestetun, Jon
453a24d7-f1b5-4dbf-b306-5ad34a53cf54
Glover, Adrian
e25fb8ce-acf2-45ae-b894-9de6d3c518e7
Georgieva, Magdalena
9e336902-08e7-4ff5-b06b-fc57c0e078d2
Taboada, Sergi
a064593b-c411-473a-ae9f-6c753ded9010
Riesgo, Ana
3e375d1f-2e40-4d69-8c11-20aaf6872bb2
Diez-Vives, Cristina
92c0ec1b-be26-48cf-abe5-4c2d6eaee6d8
De Leo, Fabio
47fce20b-71a6-440e-83fc-333cbc75cbcf
Jeffreys, Rachel
81eebb35-6ff9-4903-a2b1-39a5a3104a84
Copley, Jonathan
5f30e2a6-76c1-4150-9a42-dcfb8f5788ef
Little, Crispin
2f877300-3a98-465c-a033-ab3ac231755d
Rios, Pilar
cf976de9-bc7b-4e21-b146-89a51458fe9b
Cristobo, Javier
6eeae36a-1f42-430d-9600-995da88370d9
Hestetun, Jon
453a24d7-f1b5-4dbf-b306-5ad34a53cf54
Glover, Adrian
e25fb8ce-acf2-45ae-b894-9de6d3c518e7

Georgieva, Magdalena, Taboada, Sergi, Riesgo, Ana, Diez-Vives, Cristina, De Leo, Fabio, Jeffreys, Rachel, Copley, Jonathan, Little, Crispin, Rios, Pilar, Cristobo, Javier, Hestetun, Jon and Glover, Adrian (2020) Evidence of vent-adaptation in sponges living at the periphery of hydrothermal vent environments: Ecological and evolutionary implications. Frontiers in Microbiology, 11, [1636]. (doi:10.3389/fmicb.2020.01636).

Record type: Article

Abstract

The peripheral areas of deep-sea hydrothermal vents are often inhabited by an assemblage of animals distinct to those living close to vent chimneys. For many such taxa, it is considered that peak abundances in the vent periphery relate to the availability of hard substrate as well as the increased concentrations of organic matter generated at vents, compared to background areas. However, the peripheries of vents are less well-studied than the assemblages of vent-endemic taxa, and the mechanisms through which peripheral fauna may benefit from vent environments are generally unknown. Understanding this is crucial for evaluating the sphere of influence of hydrothermal vents and managing the impacts of future human activity within these environments, as well as offering insights into the processes of metazoan adaptation to vents. In this study, we explored the evolutionary histories, microbiomes and nutritional sources of two distantly-related sponge types living at the periphery of active hydrothermal vents in two different geological settings (Cladorhiza from the E2 vent site on the East Scotia Ridge, Southern Ocean, and Spinularia from the Endeavour vent site on the Juan de Fuca Ridge, North-East Pacific) to examine their relationship to nearby venting. Our results uncovered a close sister relationship between the majority of our E2 Cladorhiza specimens and the species Cladorhiza methanophila, known to harbor and obtain nutrition from methanotrophic symbionts at cold seeps. Our microbiome analyses demonstrated that both E2 Cladorhiza and Endeavour Spinularia sp. are associated with putative chemosynthetic Gammaproteobacteria, including Thioglobaceae (present in both sponge types) and Methylomonaceae (present in Spinularia sp.). These bacteria are closely related to chemoautotrophic symbionts of bathymodiolin mussels. Both vent-peripheral sponges demonstrate carbon and nitrogen isotopic signatures consistent with contributions to nutrition from chemosynthesis. This study expands the number of known associations between metazoans and potentially chemosynthetic Gammaproteobacteria, indicating that they can be incredibly widespread and also occur away from the immediate vicinity of chemosynthetic environments in the vent-periphery, where these sponges may be adapted to benefit from dispersed vent fluids.

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More information

Accepted/In Press date: 23 June 2020
e-pub ahead of print date: 24 July 2020
Published date: 24 July 2020
Additional Information: Copyright © 2020 Georgieva, Taboada, Riesgo, Díez-Vives, De Leo, Jeffreys, Copley, Little, Ríos, Cristobo, Hestetun and Glover.
Keywords: 16S rRNA amplicon, Porifera, chemosynthesis, cold seep, microbiome, nutrition

Identifiers

Local EPrints ID: 445363
URI: http://eprints.soton.ac.uk/id/eprint/445363
ISSN: 1664-302X
PURE UUID: ba5ead8e-4ead-4a53-8acc-704cfead91bf
ORCID for Jonathan Copley: ORCID iD orcid.org/0000-0003-3333-4325

Catalogue record

Date deposited: 04 Dec 2020 17:30
Last modified: 18 Feb 2021 16:44

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Contributors

Author: Magdalena Georgieva
Author: Sergi Taboada
Author: Ana Riesgo
Author: Cristina Diez-Vives
Author: Fabio De Leo
Author: Rachel Jeffreys
Author: Jonathan Copley ORCID iD
Author: Crispin Little
Author: Pilar Rios
Author: Javier Cristobo
Author: Jon Hestetun
Author: Adrian Glover

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