Maldonado, Manuel, Bayer, Kristina and Lopez-Acosta, Maria (2024) Nitrogen and Phosphorus Cycling Through Marine Sponges: Physiology, Cytology, Genomics, and Ecological Implications. In: Frontiers in Invertebrate Physiology: A Collection of Reviews. ; Volume 1: Non-Bilaterian Phyla , ed. by Saleuddin, Saber, Leys, Sally P., Roer, Robert D. and Wilkie, Iain C.. Apple Academic Press Inc, Palm Bay, FL, USA, pp. 197-288. ISBN 9781774914007 DOI 10.1201/9781003403319-4.

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Abstract

Several inorganic compounds of nitrogen (N) and phosphorus (P) are key to ocean ecology because, among other effects, they sustain primary production. After discovering in the 1980s that sponges can be both source and sink of such nutrients, much has been learned, including that fluxes derive from the metabolic integration of the sponge tissues and the assemblage of prokaryotic microbes living in them (i.e., the microbiota). The advent of molecular techniques revealed exceptional phylogenetic biodiversity in the microbiota and allowed the identification of genes coding for enzymes transforming N and P compounds. However, the accumulated information remains relatively inarticulate and its ecological dimension is uncharted. Herein we summarize the basics of N and P cycling in the marine environment to further address nutrient flux rates compiled from 92 sponge species. Ammonium release or 198consumption, followed by nitrite release, emerged as the most common fluxes in sponges. Phosphate release was also prevalent. A difficulty with the available information is a bias towards tropical shallow-water demosponges and the use of non-comparable units. A total of 63 prokaryotic phyla are known from sponge microbiomes. Collectively, they have the genetic potential for all aerobic and anaerobic N transformations, facilitating the formation of closed circuits for N to recycle within the holobionts (i.e., sponge + microbiota). Often, such circuits are fueled by important production/consumption of ammonium. Phosphorus cycling remains understudied, with evidence of phosphate and (organic) phosphonate utilization. Phosphate does not appear to limit sponge microbiomes, with polyphosphate (Poly-P) probably serving more as energy storage than as a P reservoir. Dissimilatory phosphite oxidation (DPO), which would explain the phosphate efflux from the sponges, has not been detected and the causes of the efflux (perhaps anoxic Poly-P degradation) remain uncertain. A relevant benefit provided by the microbiome, in addition to recycling sponge N wastes and provisioning vitamins and some organic C and N compounds through fixation, is to serve as energetically inexpensive particulate food, liberating sponges from strict dependence on inputs of external food. To facilitate co-existence and cooperation between aerobic and anaerobic microbial lineages, sponges modulate pumping activity and have evolved special cells (bacteriocytes) to enclose microbes. Species-specific metabolic integration between sponges and their microbiome yields singular holobionts with remarkable roles in the benthic-pelagic coupling of N and P cycles. Some sponge aggregations can achieve higher denitrification rates per unit area than sediments; others have higher ammonium consumption rates than eutrophic phytoplanktonic communities. Through their microbiomes, some sponge species may also cope with low oxygen conditions and modify local N and P nutrient concentrations, unchaining a cascade of ecological changes that may lead to the exclusion of competitors. Identified gaps in knowledge related to: (i) how the nutrients going in and out of the holobiont are quantitatively connected to the microbial processes occurring inside; (ii) how microbes interact with each other; and (iii) how sponges co-evolved to facilitate co-existence and functional networking in the microbiome.

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