EU project SponGES
Published July 24, 2020 | Version v1
Journal article Open

Evidence of Vent-Adaptation in Sponges Living at the Periphery of Hydrothermal Vent Environments: Ecological and Evolutionary Implications

Creators

  • 1. Life Sciences Department, Natural History Museum, London, United Kingdom
  • 2. Life Sciences Department, Natural History Museum, London, United Kingdom; Departamento de Biología (Zoología), Universidad Autónoma de Madrid, Madrid, Spain;; Departamento de Zoología y Antropología Física, Universidad de Alcalá, Madrid, Spain
  • 3. Ocean Networks Canada, University of Victoria, Victoria, BC, Canada; Department of Biology, University of Victoria, Victoria, BC, Canada
  • 4. School of Environmental Sciences, University of Liverpool, Liverpool, United Kingdom
  • 5. School of Ocean and Earth Science, University of Southampton, Southampton, United Kingdom
  • 6. Life Sciences Department, Natural History Museum, London, United Kingdom; School of Earth and Environment, University of Leeds, Leeds, United Kingdom
  • 7. Departamento de Zoología y Antropología Física, Universidad de Alcalá, Madrid, Spain; Centro Oceanográfico de Santander, Instituto Español de Oceanografía, Santander, Spain
  • 8. Departamento de Zoología y Antropología Física, Universidad de Alcalá, Madrid, Spain; Centro Oceanográfico de Gijón, Instituto Español de Oceanografía, Gijón, Spain
  • 9. NORCE Environment, Norwegian Research Centre (NORCE), Bergen, Norway

Description

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.

Notes

ACKNOWLEDGMENTS We would like to thank the crew and captains of expeditions RRS James Cook JC042, RV Polarstern PS119, RV Nautilus NA098, RV Miguel Oliver Patagonia 1208 (SGM), RV Angeles Alvariño SponGES0617 (IEO), RV G. O. Sars Mareano 113, and NOAAS Okeanos Explorer EX1711 for collections of material for this study. We are grateful to Kartin Linse and Dorte Janussen for access to JC042 Cladorhiza samples, and to Leigh Marsh and Veerle Huvenne for their help with access to JC042 data. We are also grateful to Jillian Petersen for very helpful discussions on early versions of this work, as well as to Jillian Petersen and Peter Deines for their valuable reviews of the manuscript. SUPPLEMENTARY MATERIAL The Supplementary Material for this article can be found online at: https://www.frontiersin.org/articles/10.3389/fmicb. 2020.01636/full#supplementary- material FIGURE S1 | Relative abundances (log10 transformed) of the most common prokaryotes for individual sponge samples at the genus level. Genera with relative abundances lower than 0.5% across the dataset were omitted from the figure. The heatmaps also illustrate similarity (weighted UniFrac distance cladograms) of microbiome composition for each microbiome dataset analyzed, (A) Cladorhiza-Chondrocladia (Dataset 1) and (B) Spinularia-Sycon (Dataset 2), while (C) Cladorhizidae dataset generated by Hestetun et al. (2016a) (Dataset 3). Genus and species names are abbreviated as follows: Cl. Cladorhiza, Ch. Chondrocladia, rob. robertballardi, ver. verticillata, Ly. cup. Lycopina cupressiformis, As. Asbestopluma, meth. methanophila, abyss. abyssicola, cort. corticocancellata, Spi. Spinularia, Sy. Sycon. FIGURE S2 | Carbon and nitrogen isotopic results (δ13C and δ15N) for E2 Cladorhiza and Endeavour Spinularia sp. specimens analyzed during the present study in comparison to results for cladorhizid sponges from the previous studies of Erickson et al. (2009), Reid et al. (2013), and Hestetun et al. (2016a). TABLE S1 | Primers used for amplification and sequencing of DNA fragments used in phylogenetic analyses. TABLE S2 | Genbank sequence codes of specimens used in phylogenetic analyses of Cladorhizidae. TABLE S3 | Genbank sequence codes of specimens used in phylogenetic analyses of Polymastiidae. TABLE S4 | Overview of the datasets used for 16S rRNA sequencing. TABLE S5 | COI genetic distances (p-distance) for the genus Cladorhiza. TABLE S6 | 28S genetic distances (p-distance) for the genus Cladorhiza. TABLE S7 | ALG11 genetic distances (p-distance) for the genus Cladorhiza. TABLE S8 | COI genetic distances (p-distance) for the family Polymastiidae. TABLE S9 | 28S genetic distances (p-distance) for the family Polymastiidae. TABLE S10 | Relative abundance of the 10 most common prokaryotes over the Cladorhiza-Chondrocladia dataset (Dataset 1) at the phylum, class and genus level. Values over 5% are highlighted. TABLE S11 | Relative abundance of the 10 most common prokaryotes over the Spinularia-Sycon dataset (Dataset 2) at the phylum, class and genus level. Values over 5% are highlighted. TABLE S12 | Relative abundance of the 10 most common prokaryotes over the Hestetun et al. (2016a) dataset (Dataset 3) at the phylum, class and genus level. Values over 5% are highlighted. DATA AVAILABILITY STATEMENT The datasets presented in this study can be found in online repositories. The names of the repository/repositories and accession number(s) can be found at: https://www.ncbi.nlm. nih.gov/, BioProject accession number PRJNA635099, sample accession numbers SAMN15016193 to SAMN15016217 https:// www.ncbi.nlm.nih.gov/genbank/, accession numbers MT521886 to MT521916. AUTHOR CONTRIBUTIONS MG, AR, AG, and JC conceived of the study. JC, FD, CL, PR, JC, and JH collected the specimens. MG, ST and CD performed the molecular lab work and data analysis. RJ conducted isotopic analyses. MG led the original draft preparation. All authors contributed to the writing-review and editing of the final version of the manuscript.

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Georgieva et al 2020-Data_Sheet_1_Evidence of Vent-Adaptation in Sponges Living at the Periphery of Hydrothermal Vent Environments_ Ecological and Evolutionary Implication.pdf

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Dataset: https://www.frontiersin.org/articles/10.3389/fmicb.2020.01636/full#supplementary-material (URL)
Figure: https://www.frontiersin.org/articles/10.3389/fmicb.2020.01636/full#supplementary-material (URL)
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Journal article: https://www.frontiersin.org/articles/10.3389/fmicb.2020.01636/full?report=reader#h1 (URL)

Funding

SponGES – Deep-sea Sponge Grounds Ecosystems of the North Atlantic: an integrated approach towards their preservation and sustainable exploitation 679849
European Commission