Meggie Hudspith1, Laura Rix2, Michelle Achlatis2, Jeremy Bougoure3, Paul Guagliardo3, Peta L Clode3,4,5, Nicole S Webster6,7, Gerard Muyzer8, Mathieu Pernice9, Jasper M de Goeij8,10. 1. Department of Freshwater and Marine Ecology, Institute for Biodiversity and Ecosystem Dynamics, University of Amsterdam, Amsterdam, The Netherlands. m.r.hudspith@uva.nl. 2. School of Biological Sciences, University of Queensland, Brisbane, Australia. 3. Centre for Microscopy, Characterisation and Analysis, The University of Western Australia, Perth, Australia. 4. The UWA Oceans Institute, The University of Western Australia, Perth, Australia. 5. The UWA School of Biological Sciences, The University of Western Australia, Perth, Australia. 6. Australian Institute of Marine Science, Townsville, Australia. 7. Australian Centre for Ecogenomics, University of Queensland, Brisbane, Australia. 8. Department of Freshwater and Marine Ecology, Institute for Biodiversity and Ecosystem Dynamics, University of Amsterdam, Amsterdam, The Netherlands. 9. Climate Change Cluster (C3), Faculty of Science, University of Technology, Sydney, Australia. 10. CARMABI Foundation, Piscaderabaai z/n, P.O. Box 2090, Willemstad, Curaçao.
Abstract
BACKGROUND: Sponges are increasingly recognised as key ecosystem engineers in many aquatic habitats. They play an important role in nutrient cycling due to their unrivalled capacity for processing both dissolved and particulate organic matter (DOM and POM) and the exceptional metabolic repertoire of their diverse and abundant microbial communities. Functional studies determining the role of host and microbiome in organic nutrient uptake and exchange, however, are limited. Therefore, we coupled pulse-chase isotopic tracer techniques with nanoscale secondary ion mass spectrometry (NanoSIMS) to visualise the uptake and translocation of 13C- and 15N-labelled dissolved and particulate organic food at subcellular level in the high microbial abundance sponge Plakortis angulospiculatus and the low microbial abundance sponge Halisarca caerulea. RESULTS: The two sponge species showed significant enrichment of DOM- and POM-derived 13C and 15N into their tissue over time. Microbial symbionts were actively involved in the assimilation of DOM, but host filtering cells (choanocytes) appeared to be the primary site of DOM and POM uptake in both sponge species overall, via pinocytosis and phagocytosis, respectively. Translocation of carbon and nitrogen from choanocytes to microbial symbionts occurred over time, irrespective of microbial abundance, reflecting recycling of host waste products by the microbiome. CONCLUSIONS: Here, we provide empirical evidence indicating that the prokaryotic communities of a high and a low microbial abundance sponge obtain nutritional benefits from their host-associated lifestyle. The metabolic interaction between the highly efficient filter-feeding host and its microbial symbionts likely provides a competitive advantage to the sponge holobiont in the oligotrophic environments in which they thrive, by retaining and recycling limiting nutrients. Sponges present a unique model to link nutritional symbiotic interactions to holobiont function, and, via cascading effects, ecosystem functioning, in one of the earliest metazoan-microbe symbioses. Video abstract.
BACKGROUND: Sponges are increasingly recognised as key ecosystem engineers in many aquatic habitats. They play an important role in nutrient cycling due to their unrivalled capacity for processing both dissolved and particulate organic matter (DOM and POM) and the exceptional metabolic repertoire of their diverse and abundant microbial communities. Functional studies determining the role of host and microbiome in organic nutrient uptake and exchange, however, are limited. Therefore, we coupled pulse-chase isotopic tracer techniques with nanoscale secondary ion mass spectrometry (NanoSIMS) to visualise the uptake and translocation of 13C- and 15N-labelled dissolved and particulate organic food at subcellular level in the high microbial abundance sponge Plakortis angulospiculatus and the low microbial abundance sponge Halisarca caerulea. RESULTS: The two sponge species showed significant enrichment of DOM- and POM-derived 13C and 15N into their tissue over time. Microbial symbionts were actively involved in the assimilation of DOM, but host filtering cells (choanocytes) appeared to be the primary site of DOM and POM uptake in both sponge species overall, via pinocytosis and phagocytosis, respectively. Translocation of carbon and nitrogen from choanocytes to microbial symbionts occurred over time, irrespective of microbial abundance, reflecting recycling of host waste products by the microbiome. CONCLUSIONS: Here, we provide empirical evidence indicating that the prokaryoticcommunities of a high and a low microbial abundance sponge obtain nutritional benefits from their host-associated lifestyle. The metabolic interaction between the highly efficient filter-feeding host and its microbial symbionts likely provides a competitive advantage to the sponge holobiont in the oligotrophic environments in which they thrive, by retaining and recycling limiting nutrients. Sponges present a unique model to link nutritional symbiotic interactions to holobiont function, and, via cascading effects, ecosystem functioning, in one of the earliest metazoan-microbe symbioses. Video abstract.
Authors: Brittany E Alexander; Kevin Liebrand; Ronald Osinga; Harm G van der Geest; Wim Admiraal; Jack P M Cleutjens; Bert Schutte; Fons Verheyen; Marta Ribes; Emiel van Loon; Jasper M de Goeij Journal: PLoS One Date: 2014-10-07 Impact factor: 3.240
Authors: Meggie Hudspith; Jasper M de Goeij; Mischa Streekstra; Niklas A Kornder; Jeremy Bougoure; Paul Guagliardo; Sara Campana; Nicole N van der Wel; Gerard Muyzer; Laura Rix Journal: ISME J Date: 2022-06-02 Impact factor: 11.217