Subcellular view of host\u2013microbiome nutrient exchange in sponges: insights into the ecological success of an early metazoan\u2013microbe symbiosis

Meggie Hudspith,Jasper M De Goeij,Nicole S Webster,Mathieu Pernice,Laura Rix,Peta L Clode,Paul Guagliardo,Gerard Muyzer,Michelle Achlatis,Jeremy Bougoure

doi:10.1186/s40168-020-00984-w

Abstract

BackgroundSponges 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.ResultsThe 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.ConclusionsHere, 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.1KyCQaknthx73_ZUqh3faYVideo abstract

Highlights

Sponges are increasingly recognised as key ecosystem engineers in many aquatic habitats
The rate of 13C incorporation during the pulse phase was significantly higher for the low microbial abundance (LMA) species H. caerulea than for the high microbial abundance (HMA) species P. angulospiculatus (ANOVA, F = 10.54, df = 1, p = 0.003) and the inverse relationship was true for 15N incorporation (ANOVA, F = 5.5, df = 1, p = 0.027)
Particulate organic matter (POM) Both P. angulospiculatus and H. caerulea showed a linear increase of POM-derived 13C- and 15N-enrichment into their tissue during the 3-h pulse phase, but the HMA species P. angulospiculatus incorporated POM at a significantly lower rate than the LMA species H. caerulea for both 13C and 15N (ANOVA, F = 11.13 and p = 0.003, F = 11.34 and p = 0.002 for 13C and 15N, respectively) and enrichment was low across the pulsechase experiment (Fig. 2c, d)

Summary

Introduction

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. Sponges are increasingly recognised as key ecosystem engineers in many aquatic habitats, playing important roles in ecological processes, such as habitat provision and nutrient cycling [1, 2]. As filter-feeders par excellence [3, 4], the ecological success of sponges largely depends upon their ability to capture and transform a suite of organic and inorganic nutrients Their unique and varied diet is related to the (inter)activity of the sponge host and its abundant and diverse microbial community, collectively termed the sponge holobiont. In the deep-sea sponge Geodia barretti, microbially mediated nitrogen transformations were suggested to be fuelled by metabolic waste products of the host [28], but without direct evidence

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