Description: 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.

Description: Hexactinellid sponges are common in the deep sea, but their functional integration into those ecosystems remains poorly understood. The phylogenetically related species Schaudinnia rosea and Vazella pourtalesii were herein incubated for nitrogen and phosphorous, returning markedly different nutrient fluxes. Transmission electron microscopy (TEM) revealed S. rosea to host a low abundance of extracellular microbes, while Vazella pourtalesii showed higher microbial abundance and hosted most microbes within bacteriosyncytia, a novel feature for Hexactinellida. Amplicon sequences of the microbiome corroborated large between-species differences, also between the sponges and the seawater of their habitats. Metagenome-assembled genome of the V. pourtalesii microbiota revealed genes coding for enzymes operating in nitrification, denitrification, dissimilatory nitrate reduction to ammonium, nitrogen fixation, and ammonia/ammonium assimilation. In the nitrification and denitrification pathways some enzymes were missing, but alternative bridging routes allow the microbiota to close a N cycle in the holobiont. Interconnections between aerobic and anaerobic pathways may facilitate the sponges to withstand the low-oxygen conditions of deep-sea habitats. Importantly, various N pathways coupled to generate ammonium, which, through assimilation, fosters the growth of the sponge microbiota. TEM showed that the farmed microbiota is digested by the sponge cells, becoming an internal food source. This microbial farming demands more ammonium that can be provided internally by the host sponges and some 2.6 million kg of ammonium from the seawater become annually consumed by the aggregations of V. pourtalesii. Such ammonium removal is likely impairing the development of the free-living bacterioplankton and the survival chances of other sponge species that feed on bacterioplankton. Such nutritional competitive exclusion would favor the monospecific character of the V. pourtalesii aggregations. These aggregations also affect the surrounding environment through an annual release of 27.3 million kg of nitrite and, in smaller quantities, of nitrate and phosphate. The complex metabolic integration among the microbiota and the sponge suggests that the holobiont depends critically on the correct functioning of its N-driven microbial engine. The metabolic intertwining is so delicate that it changed after moving the sponges out of their habitat for a few days, a serious warning on the conservation needs of these sponge aggregations.

Description: Dissolved silicon is an essential nutrient for the growth of various ocean organisms that need it to build their skeletons. Most of the dissolved silicon that sustains these organisms comes from the breakdown of silicon-containing rocks on land. In recent decades, human activities have greatly disturbed the transport of silicon from land to ocean. For example, dams built to generate electricity can interrupt the transport of dissolved silicon and starve downstream areas. Fertilizers and other human pollution add large amounts of non-silicon nutrients to rivers, lakes, and reservoirs, which can stimulate organisms to grow and use up silicon before it reaches the ocean. In addition, consequences of climate change can also impact the silicon cycle. In this article, we explain how human activities have disturbed the silicon cycle and discuss how climate change may affect it in the future.

Description: Silicon is one of the most abundant chemical elements in the universe. On Earth, it forms sediments, minerals, and rocks. In the ocean, silicon is found in a dissolved form that can be used by many organisms to grow. You probably know that humans use calcium to build their skeletons, but did you know that there are creatures capable of forming skeletons out of silicon? Organisms capable of capturing dissolved silicon from the environment and transforming it into glassy skeletons are called silicifiers. Silicifiers use a unique process called biosilicification to create their skeletons. In the marine ecosystem, silicifiers come in a surprising variety of shapes and sizes, and they include, among others, diatoms, rhizarians, and sponges. These three groups, so diverse and yet so similar, are essential to the health of the oceans.

Description: © The Author(s), 2021. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Treguer, P. J., Sutton, J. N., Brzezinski, M., Charette, M. A., Devries, T., Dutkiewicz, S., Ehlert, C., Hawkings, J., Leynaert, A., Liu, S. M., Monferrer, N. L., Lopez-Acosta, M., Maldonado, M., Rahman, S., Ran, L., & Rouxel, O. Reviews and syntheses: the biogeochemical cycle of silicon in the modern ocean. Biogeosciences, 18(4), (2021): 1269-1289, https://doi.org/10.5194/bg-18-1269-2021.

Description: The element silicon (Si) is required for the growth of silicified organisms in marine environments, such as diatoms. These organisms consume vast amounts of Si together with N, P, and C, connecting the biogeochemical cycles of these elements. Thus, understanding the Si cycle in the ocean is critical for understanding wider issues such as carbon sequestration by the ocean's biological pump. In this review, we show that recent advances in process studies indicate that total Si inputs and outputs, to and from the world ocean, are 57 % and 37 % higher, respectively, than previous estimates. We also update the total ocean silicic acid inventory value, which is about 24 % higher than previously estimated. These changes are significant, modifying factors such as the geochemical residence time of Si, which is now about 8000 years, 2 times faster than previously assumed. In addition, we present an updated value of the global annual pelagic biogenic silica production (255 Tmol Si yr−1) based on new data from 49 field studies and 18 model outputs, and we provide a first estimate of the global annual benthic biogenic silica production due to sponges (6 Tmol Si yr−1). Given these important modifications, we hypothesize that the modern ocean Si cycle is at approximately steady state with inputs =14.8(±2.6) Tmol Si yr−1 and outputs =15.6(±2.4) Tmol Si yr−1. Potential impacts of global change on the marine Si cycle are discussed.

Description: This work was supported by the French National Research Agency (18-CEO1-0011-01) and by the Spanish Ministry of Science, Innovation and Universities (PID2019-108627RB-I00).