Subcellular view of host–microbiome nutrient exchange in sponges: insights into the ecological success of an early metazoan–microbe symbiosis

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.