Broad Phylogenetic Occurrence of the Oxygen-Binding Hemerythrins in Bilaterians

Abstract

Animal tissues need to be properly oxygenated for carrying out catabolic respiration and, as such, natural selection has presumably favored special molecules that can reversibly bind and transport oxygen. Hemoglobins, hemocyanins, and hemerythrins (Hrs) fulfill this role, with Hrs being the least studied. Knowledge of oxygen-binding proteins is crucial for understanding animal physiology. Hr genes are present in the three domains of life, Archaea, Bacteria, and Eukaryota; however, within Animalia, Hrs has been reported only in marine species in six phyla (Annelida, Brachiopoda, Priapulida, Bryozoa, Cnidaria, and Arthropoda). Given this observed Hr distribution, whether all metazoan Hrs share a common origin is circumspect. We investigated Hr diversity and evolution in metazoans, by employing in silico approaches to survey for Hrs from of 120 metazoan transcriptomes and genomes. We found 58 candidate Hr genes actively transcribed in 36 species distributed in 11 animal phyla, with new records in Echinodermata, Hemichordata, Mollusca, Nemertea, Phoronida, and Platyhelminthes. Moreover, we found that “Hrs” reported from Cnidaria and Arthropoda were not consistent with that of other metazoan Hrs. Contrary to previous suggestions that Hr genes were absent in deuterostomes, we find Hr genes present in deuterostomes and were likely present in early bilaterians, but not in nonbilaterian animal lineages. As expected, the Hr gene tree did not mirror metazoan phylogeny, suggesting that Hrs evolutionary history was complex and besides the oxygen carrying capacity, the drivers of Hr evolution may also consist of secondary functional specializations of the proteins, like immunological functions.

Examining the role of oxygen-binding proteins on the early evolution of multicellularity

“…We therefore suggest an alternative hypothesis for the role and timing of the origins of oxygen-binding proteins in the animal lineage: that they may have evolved in response to rising oxygen levels in the environment, allowing larger multicellular organisms to then exploit the increased metabolic potential of abundant environmental oxygen. Our hypothesis is consistent with the fact that oxygen binding globins and hemerythrins appear to have an origin circa the common ancestor of bilateria [17,19,[29][30][31]. These proteins also first originate in the Ediacaran period, after the Neoproterozoic oxygenation event in which oxygen levels rose to near today's values [40,52].…”

“…However, phylogenetic studies tracing the origins of animal respiratory proteins reveal that freely circulating oxygen carriers with cooperative oxygen binding in blood and hemolymph evolved well after the origin of macroscopic size, and are in fact derived from more ancient monomeric stationary globins and hemerythrins that were not transported in circulatory fluids [17][18][19][20]. These more primitive proteins were expressed in body cells and tissues, but still served to facilitate oxygen diffusion from cell to cell and through tissues by increasing the effective diffusion rate of oxygen much as modern tissue globins such as myoglobin do today [21][22][23][24][25][26][27][28].…”

“…These more primitive proteins were expressed in body cells and tissues, but still served to facilitate oxygen diffusion from cell to cell and through tissues by increasing the effective diffusion rate of oxygen much as modern tissue globins such as myoglobin do today [21][22][23][24][25][26][27][28]. The ancestral genes encoding these simple intracellular oxygen diffusion facilitators likely originated prior to most recent common ancestor of bilateria [17,19,[29][30][31], a critical clade in animal evolution which is defined by the origin of triploblastic embryos with endoderm, ectoderm and mesoderm germ layers which give rise to complex tissues more than two cells thick [32].…”

Uncharted biodiversity in the marine benthos: the void of the smallish with description of ten new Platyhelminth taxa from the well-studied North Sea

“…Dactyloplana tridigitata lives in fine to medium subtidal sand and was only found in cores penetrating deeper than 10 cm into the sediment, together with a number of other red-coloured platyhelminths (Pseudoschizorhynchoides ruber, Subulagera rubra, Diascorhynchus rubrus). Presumably it is specialised for larger sediment depth or low oxygen conditions and the red stain is oxygen-binding hemerythrin allowing oxygendependent organisms to temporarily enter low-oxygen or anoxic habitats [40].…”