Evolutionary History of the Globin Gene Family in Annelids

Abstract

Animals depend on the sequential oxidation of organic molecules to survive; thus, oxygen-carrying/transporting proteins play a fundamental role in aerobic metabolism. Globins are the most common and widespread group of respiratory proteins. They can be divided into three types: circulating intracellular, non-circulating intracellular, and extracellular, all of which have been reported in annelids. The diversity of oxygen transport proteins has been underestimated across metazoans. We probed 250 annelid transcriptomes in search of globin diversity in order to elucidate the evolutionary history of this gene family within this phylum. We report two new globin types in annelids, namely androglobins and cytoglobins. Although cytoglobins and myoglobins from vertebrates and from invertebrates are referred to by the same name, our data show they are not genuine orthologs. Our phylogenetic analyses show that extracellular globins from annelids are more closely related to extracellular globins from other metazoans than to the intracellular globins of annelids. Broadly, our findings indicate that multiple gene duplication and neo-functionalization events shaped the evolutionary history of the globin family.

Globins in the marine annelid Platynereis dumerilii shed new light on hemoglobin evolution in bilaterians

“…In annelids, our phylogenetic analysis is in accordance with the scenario that early gene duplications, probably in the last common ancestor of modern annelids, produced the initial two families (A, B) encompassing the four extracellular globin sub-families A1, A2, B1, B2 that form the HBL-Hb. A recent work based on a massive sampling of annelid species transcriptomes recovered a variable number of extracellular globins, ranging from 1 to 12 depending on the species [ 7 , 19 ]. Gene trees made in this later work suggest that, while the early gene duplication A/B indeed occurred prior to annelid diversification, the sub-families A1, A2, B1 and B2 are not recognizable at the scale of the annelid tree.…”

“…These studies emphasize the universality of the globin fold motif present since the last common ancestor of all living cells (LUCA, last universal common ancestor) and the likely functions of these proteins as enzymes or sensors. Within metazoans, many works have analyzed globin evolution in specific metazoan groups such as annelids [ 6 , 7 ], deuterostomes [ 8 ], echinoderms [ 9 ], pancrustaceans [ 10 ], insects [ 11 ], cephalochordates [ 12 ], chordates [ 13 ] or agnathans [ 14 , 15 ].…”

Chromosome-scale genome assembly and gene annotation of the hydrothermal vent annelidAlvinella pompejanayield insight into animal evolution in extreme environments

“…In common with other annelids [69,70], the Alvinella genome encodes a high number of globin genes, predicted to include both intra- and extra-cellular proteins. We detected 2 genomic clusters of globins corresponding to Alvinella pompejana specific gene duplications.…”

Comparison of Evolutionary Relationships between Branchiostoma floridae, Ciona intestinalis, and Homo sapiens Globins Provide Evidence of Gene Co-Option and Convergent Evolution

“…Although the physiological functions of extracellular hemoglobin released by the hemolysis of red blood cells have been discussed [32], no secretion of globin protein, which has a signal peptide sequence, has been reported in vertebrates. On the other hand, in the vascular fluid, hemolymph, or coelomic fluid of some invertebrate phyla, including Annelida, Nematoda, Arthropoda, and Mollusca [33,34], extracellular hemoproteins of various forms and sizes such as monomeric hemoglobin and giant (ca. 3600 kDa) hexagonal bilayer hemoglobin have been reported [35].…”