Divalent metal transporter-related protein restricts animals to marine habitats

Abstract

Utilization and regulation of metals from seawater by marine organisms are important physiological processes. To better understand metal regulation, we searched the crown-of-thorns starfish genome for the divalent metal transporter (DMT) gene, a membrane protein responsible for uptake of divalent cations. We found two DMT-like sequences. One is an ortholog of vertebrate DMT, but the other is an unknown protein, which we named DMT-related protein (DMTRP). Functional analysis using a yeast expression system demonstrated that DMT transports various metals, like known DMTs, but DMTRP does not. In contrast, DMTRP reduced the intracellular concentration of some metals, especially zinc, suggesting its involvement in negative regulation of metal uptake. Phylogenetic distribution of the DMTRP gene in various metazoans, including sponges, protostomes, and deuterostomes, indicates that it originated early in metazoan evolution. However, the DMTRP gene is only retained in marine species, and its loss seems to have occurred independently in ecdysozoan and vertebrate lineages from which major freshwater and land animals appeared. DMTRP may be an evolutionary and ecological limitation, restricting organisms that possess it to marine habitats, whereas its loss may have allowed other organisms to invade freshwater and terrestrial habitats.

Nramp: Deprive and conquer?

“…First there was selection for coupled uptake of Mn 2+ and H + ; with aerobiosis onset and increased respiratory rate an alternative H + uptake pathway was accommodated (uncoupling), then modified in archaeal pre-eukaryotic cells and completed in FECA. This suggests that stepwise evolution of Slc11 phylogroups reflects functional adaptations to environmental changes ( Sassa et al, 2021 ), including the chemical (ΔpH) and electrical (ΔΨ) components of the H + electrochemical gradient of their respective membrane.…”

Emergence of Slc11 clade MCbgut: a parsimonious hypothesis for the dawn of Lactobacillales in the gut of early vertebrates

“…But this possibility may provide an interesting angle to approach our intimate relationships with LB because vertebrate development owed to successive innovations following differentiation of the pharynx at the entry of the digestive tract in chordates, including for instance the development of sensory organs and vertebrate novelties such as the spleen, individualized pancreas, heart innervation and eye's own muscles [38], [39], which might have fostered mutualistic interactions between emerging LB and their host. Vertebrate inventions took place around the 1R whole genome duplication (WGD) that occurred in the early Cambrian and which produced, in particular, the archetype Nramp 'Ohnologs' Nramp1 and Dmt1 ( [40], [41], [42] and Figure S8). NRAMP1 (SLC11A1) expression depends on C/EBP [43], [44] and dominates in the spleen, blood and tissue phagocytes, contributing to host resistance to infection [8], [45].…”

“…Vertebrate inventions took place around the 1R whole genome duplication (WGD) that occurred in the early Cambrian and which produced, in particular, the archetype Nramp ‘Ohnologs’ Nramp1 and Dmt1 ([40], [41], [42] and Figure S8). NRAMP1 ( SLC11A1 ) expression depends on C/EBP [43], [44] and dominates in the spleen, blood and tissue phagocytes, contributing to host resistance to infection [8], [45].…”