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

Abstract

Background How vascular systems and their respiratory pigments evolved is still debated. While many animals present a vascular system, hemoglobin exists as a blood pigment only in a few groups (vertebrates, annelids, a few arthropod and mollusk species). Hemoglobins are formed of globin sub-units, belonging to multigene families, in various multimeric assemblages. It was so far unclear whether hemoglobin families from different bilaterian groups had a common origin. Results To unravel globin evolution in bilaterians, we studied the marine annelid Platynereis dumerilii, a species with a slow evolving genome. Platynereis exhibits a closed vascular system filled with extracellular hemoglobin. Platynereis genome and transcriptomes reveal a family of 19 globins, nine of which are predicted to be extracellular. Extracellular globins are produced by specialized cells lining the vessels of the segmental appendages of the worm, serving as gills, and thus likely participate in the assembly of a previously characterized annelid-specific giant hemoglobin. Extracellular globin mRNAs are absent in smaller juveniles, accumulate considerably in growing and more active worms and peak in swarming adults, as the need for O2 culminates. Next, we conducted a metazoan-wide phylogenetic analysis of globins using data from complete genomes. We establish that five globin genes (stem globins) were present in the last common ancestor of bilaterians. Based on these results, we propose a new nomenclature of globins, with five clades. All five ancestral stem-globin clades are retained in some spiralians, while some clades disappeared early in deuterostome and ecdysozoan evolution. All known bilaterian blood globin families are grouped in a single clade (clade I) together with intracellular globins of bilaterians devoid of red blood. Conclusions We uncover a complex “pre-blood” evolution of globins, with an early gene radiation in ancestral bilaterians. Circulating hemoglobins in various bilaterian groups evolved convergently, presumably in correlation with animal size and activity. However, all hemoglobins derive from a clade I globin, or cytoglobin, probably involved in intracellular O2 transit and regulation. The annelid Platynereis is remarkable in having a large family of extracellular blood globins, while retaining all clades of ancestral bilaterian globins.

MorphoFeatures for unsupervised exploration of cell types, tissues, and organs in volume electron microscopy

“…Cluster 1 shows specific expression of the homeodomain transcription factors lhx6 and phox2 and an ap2 family member, while cluster 6 composed of dark neurosecretory cells shows specific expression of two neurosecretion markers, atrial natriuretic peptide receptor anpra and prohormone convertase phc2 , identifying these as brain parts of the circular and apical nervous system, respectively ( Vergara et al, 2021 ; Arendt, 2021 ). Cluster 8, another neural cluster, is enriched for the oxidative stress marker cytoglobin ( globin-like ; Song et al, 2020 ) and the bHLH transcription factor mitf . Subclustering revealed three subclusters, one of which represents rhabdomeric photoreceptors of the adult eye ( Figure 3B , subcluster 8.1) that specifically express mitf and globin-like .…”

MorphoFeatures: unsupervised exploration of cell types, tissues and organs in volume electron microscopy

“…Cluster 1 shows specific expression of the homeodomain transcription factors lhx6 and phox2 and an ap2 family member, while cluster 6 composed of dark neurosecretory cells shows specific expression of two neurosecretion markers, atrial natriuretic peptide receptor anpra and prohormone convertase phc2 , identifying these as brain parts of the circular and apical nervous system, respectively ( Vergara et al (2021) ; Arendt (2021) ). Cluster 8, another neural cluster, is enriched for the oxidative stress marker cytoglobin ( globin-like ) ( Song et al (2020) ) and the bHLH transcription factor mitf . Subclustering revealed 3 subclusters, one of which represents rhabdomeric photoreceptors of the adult eye (Figure 4B, subcluster 8.1) that specifically express mitf and globin-like .…”

“…(2021); Arendt (2021)). Cluster 8, another neural cluster, is enriched for the oxidative stress marker cytoglobin (globin-like)(Song et al (2020)) and the bHLH transcription factor mitf. Subclustering revealed 3 subclusters, one of which represents rhabdomeric photoreceptors of the adult eye (Figure4B, subcluster 8.1) that specifically express mitf and globin-like.…”

Whole-Genome Duplications and the Diversification of the Globin-X Genes of Vertebrates

“…Because these analyses included highly contiguous cyclostome genomes plus newly released genomes from cartilaginous fish as well as representatives of the deepest-branching lineages of ray-finned fishes ( Du et al 2020 ; Bi et al 2021 ), we were able to resolve longstanding questions regarding the early stages of evolution of GbX genes in vertebrates. Since the time of its initial discovery ( Roesner et al 2005 ), GbX went from being an obscure gene found in a very limited sample of vertebrates to becoming a credible candidate to provide clues about the functional role of the ancestor of all animal globins ( Blank et al 2011 ; Song et al 2020 ). This paradigm change came with an increased interest in deciphering its evolutionary history and its still elusive functional role ( Burmester and Hankeln 2014 ; Keppner et al 2020 ).…”