Evidence for a Large Expansion and Subfunctionalization of Globin Genes in Sea Anemones.

Hayden L Smith,Joachim M Surm,Peter J Prentis,Matthew J Phillips,Ana Pavasovic,B Venkatesh

doi:10.1093/gbe/evy128

Hayden L Smith, Joachim M Surm + Show 4 more

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https://doi.org/10.1093/gbe/evy128

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Abstract

The globin gene superfamily has been well-characterized in vertebrates, however, there has been limited research in early-diverging lineages, such as phylum Cnidaria. This study aimed to identify globin genes in multiple cnidarian lineages, and use bioinformatic approaches to characterize the evolution, structure, and expression of these genes. Phylogenetic analyses and in silico protein predictions showed that all cnidarians have undergone an expansion of globin genes, which likely have a hexacoordinate protein structure. Our protein modeling has also revealed the possibility of a single pentacoordinate globin lineage in anthozoan species. Some cnidarian globin genes displayed tissue and development specific expression with very few orthologous genes similarly expressed across species. Our phylogenetic analyses also revealed that eumetazoan globin genes form a polyphyletic relationship with vertebrate globin genes. Overall, our analyses suggest that a Ngb-like and GbX-like gene were most likely present in the globin gene repertoire for the last common ancestor of eumetazoans. The identification of a large-scale expansion and subfunctionalization of globin genes in actiniarians provides an excellent starting point to further our understanding of the evolution and function of the globin gene superfamily in early-diverging lineages.

Highlights

Globins are among the most studied gene superfamilies, and their evolution, structure, and expression is well-established in vertebrates
Lechauve et al (2013) have shown globin genes from phyla Cnidaria, Placozoa, and Porifera form a polyphyletic relationship with globin genes from vertebrate taxa
Our data supports the findings of Lechauve et al (2013) that globin genes from early-diverging taxa do not form a single clade with vertebrate Ngb genes

Summary

Introduction

Globins are among the most studied gene superfamilies, and their evolution, structure, and expression is well-established in vertebrates (subphylum Vertebrata). Phylogenetic analyses have demonstrated that either neuroglobin (Ngb), globin-X (GbX), or androglobin is the most ancient globin gene in vertebrates and metazoans in general (Burmester and Hankeln 2014) Of note, these three ancient globin proteins and cytoglobin have a hexacoordinate structural conformation, whereas, pentacoordination is observed in the seven other globin protein subfamilies (Burmester and Hankeln 2014). These three ancient globin proteins and cytoglobin have a hexacoordinate structural conformation, whereas, pentacoordination is observed in the seven other globin protein subfamilies (Burmester and Hankeln 2014) This variation in protein structure changes the binding position of the heme molecule and ligand binding affinities to various gaseous compounds (Dewilde et al 2001; Nienhaus et al 2004; Brunori et al 2005; Fago et al 2006; Jayaraman et al 2011). These characteristics are well defined in vertebrates, this is not the case for metazoan lineages outside of vertebrates, especially for early-diverging lineages, such as cnidarians

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