EU project SponGES
Published July 8, 2020 | Version v1
Journal article Open

Cooperation between passive and active silicon transporters clarifies the ecophysiology and evolution of biosilicification in sponges

Creators

  • 1. Department of Marine Ecology, Center for Advanced Studies of Blanes (CEAB-CSIC), Acceso Cala St. Francesc 14, Blanes 17300, Girona, Spain
  • 2. Department of Fisheries and Oceans, Bedford Institute of Oceanography, 1 Challenger Dr., Dartmouth, NS, Canada
  • 3. Department of Life Sciences, The Natural History Museum of London, Cromwell Road, SW7 5BD London, UK

Description

ABSTRACT

The biological utilization of dissolved silicon (DSi) influences ocean ecology and biogeochemistry. In the deep sea, hexactinellid sponges are major DSi consumers that remain poorly understood. Their DSi consumption departs from the Michaelis-Menten kinetics of shallow-water demosponges and appears particularly maladapted to incorporating DSi from the modest concentrations typical of the modern ocean. Why did sponges not adapt to the shrinking DSi availability that followed diatom expansion some 100 to 65 million years ago? We propose that sponges incorporate DSi combining passive (aquaglyceroporins) and active (ArsB) transporters, while only active transporters (SITs) operate in diatoms and choanoflagellates. Evolution of greater silicon transport efficiency appears constrained by the additional role of aquaglyceroporins in transporting essential metalloids other than silicon. We discuss the possibility that lower energy costs may have driven replacement of ancestral SITs by less efficient aquaglyceroporins, and discuss the functional implications of conservation of aquaglyceroporin-mediated DSi utilization in vertebrates.

Notes

ACKNOWLEDGEMENTS We thank B. MacDonald for help with logistics during sponge collection and maintenance in experimental conditions, C. Sitjà for help with sponge dry and ash weights, and M. García-Puig for video editing; F. Whoriskey and J. Pratt of the (OTN, Dalhousie University) for the collection of specimens from the OTN moorings; G. Yahel (Ruppin Academic Center) for advice when building the seawater collectors of the incubation chambers. FUNDING This research was completed mostly by funds from the SponGES H2020 grant (BG-01-2015.2, agreement number 679849-2) to M.M. and A.R. and from Fisheries and Oceans Canada Strategic Program for Ecosystem-Based Research and Advice (SPERA) and International Governance Strategy (IGS) projects awarded to L.B. and E.K. This study also benefitted from funding by a PBS grant (MINECO CTM2015-67221-R) to M.M. This study is in memory of Hans Tore Rapp, who passed away on 7 March 2020, and who was the main coordinator of the H2020 SponGES project that has made this research possible. AUTHOR CONTRIBUTIONS M.M. designed the study. The physiological experiments and nutrient analyses were performed and analyzed by M.M. and M.L.-A. E.K. and L.B. dealt with mapping, collection of organisms, and the logistics of cruise organization and laboratory gearing for in vivo experimentation with deep-sea sponges and nutrient analysis. A.R. and V.K. conducted the transcriptomic analysis, the analysis of differential gene expression, and the phylogenetic analyses, being the molecular data interpreted by M.M. and A.R. M.M. assembled the first draft of manuscript, which was further refined through invaluable contributions by all authors. COMPETING INTERESTS The authors declare that they have no competing interests. DATA AND MATERIALS AVAILABILITY All data and access numbers needed to evaluate the conclusions in the paper are present in the paper and/or the Supplementary Materials. Raw transcript reads can be accessioned at the SRA under BioProject number PRJNA580361. Additional data related to this paper may be requested from the authors.

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Additional details

Related works

Is identical to
Journal article: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7439455/ (URL)
Is supplemented by
Dataset: http://advances.sciencemag.org/cgi/content/full/6/28/eaba9322/DC1 (URL)

Funding

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