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Cooperation between passive and active silicon transporters clarifies the ecophysiology and evolution of biosilicification in sponges.

ABSTRACT: The biological utilization of dissolved silicon (DSi) influences ocean ecology and biogeochemistry. In the deep sea, hexactinellid sponges are major DSi consumers that remain poorly understood. Their DSi consumption departs from the Michaelis-Menten kinetics of shallow-water demosponges and appears particularly maladapted to incorporating DSi from the modest concentrations typical of the modern ocean. Why did sponges not adapt to the shrinking DSi availability that followed diatom expansion some 100 to 65 million years ago? We propose that sponges incorporate DSi combining passive (aquaglyceroporins) and active (ArsB) transporters, while only active transporters (SITs) operate in diatoms and choanoflagellates. Evolution of greater silicon transport efficiency appears constrained by the additional role of aquaglyceroporins in transporting essential metalloids other than silicon. We discuss the possibility that lower energy costs may have driven replacement of ancestral SITs by less efficient aquaglyceroporins, and discuss the functional implications of conservation of aquaglyceroporin-mediated DSi utilization in vertebrates.

SUBMITTER: Maldonado M

PROVIDER: S-EPMC7439455 | biostudies-literature | 2020 Jul

REPOSITORIES: biostudies-literature

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Cooperation between passive and active silicon transporters clarifies the ecophysiology and evolution of biosilicification in sponges.

Maldonado M M López-Acosta M M Beazley L L Kenchington E E Koutsouveli V V Riesgo A A

Science advances 20200708 28

The biological utilization of dissolved silicon (DSi) influences ocean ecology and biogeochemistry. In the deep sea, hexactinellid sponges are major DSi consumers that remain poorly understood. Their DSi consumption departs from the Michaelis-Menten kinetics of shallow-water demosponges and appears particularly maladapted to incorporating DSi from the modest concentrations typical of the modern ocean. Why did sponges not adapt to the shrinking DSi availability that followed diatom expansion some ...[more]

PMID: 32832609

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Project description:UNLABELLED:The "Candidatus Synechococcus spongiarum" group includes different clades of cyanobacteria with high 16S rRNA sequence identity (~99%) and is the most abundant and widespread cyanobacterial symbiont of marine sponges. The first draft genome of a "Ca. Synechococcus spongiarum" group member was recently published, providing evidence of genome reduction by loss of genes involved in several nonessential functions. However, "Ca. Synechococcus spongiarum" includes a variety of clades that may differ widely in genomic repertoire and consequently in physiology and symbiotic function. Here, we present three additional draft genomes of "Ca. Synechococcus spongiarum," each from a different clade. By comparing all four symbiont genomes to those of free-living cyanobacteria, we revealed general adaptations to life inside sponges and specific adaptations of each phylotype. Symbiont genomes shared about half of their total number of coding genes. Common traits of "Ca. Synechococcus spongiarum" members were a high abundance of DNA modification and recombination genes and a reduction in genes involved in inorganic ion transport and metabolism, cell wall biogenesis, and signal transduction mechanisms. Moreover, these symbionts were characterized by a reduced number of antioxidant enzymes and low-weight peptides of photosystem II compared to their free-living relatives. Variability within the "Ca. Synechococcus spongiarum" group was mostly related to immune system features, potential for siderophore-mediated iron transport, and dependency on methionine from external sources. The common absence of genes involved in synthesis of residues, typical of the O antigen of free-living Synechococcus species, suggests a novel mechanism utilized by these symbionts to avoid sponge predation and phage attack. IMPORTANCE:While the Synechococcus/Prochlorococcus-type cyanobacteria are widely distributed in the world's oceans, a subgroup has established its niche within marine sponge tissues. Recently, the first genome of sponge-associated cyanobacteria, "Candidatus Synechococcus spongiarum," was described. The sequencing of three representatives of different clades within this cyanobacterial group has enabled us to investigate intraspecies diversity, as well as to give a more comprehensive understanding of the common symbiotic features that adapt "Ca. Synechococcus spongiarum" to its life within the sponge host.

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Cooperation between passive and active silicon transporters clarifies the ecophysiology and evolution of biosilicification in sponges.

Publications

Cooperation between passive and active silicon transporters clarifies the ecophysiology and evolution of biosilicification in sponges.

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