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. 2014 Oct;31(10):2708-21.
doi: 10.1093/molbev/msu216. Epub 2014 Jul 23.

The globin gene repertoire of lampreys: convergent evolution of hemoglobin and myoglobin in jawed and jawless vertebrates

Kim Schwarze  1 , Kevin L Campbell  2 , Thomas Hankeln  3 , Jay F Storz  4 , Federico G Hoffmann  5 , Thorsten Burmester  6
Affiliations

The globin gene repertoire of lampreys: convergent evolution of hemoglobin and myoglobin in jawed and jawless vertebrates

Kim Schwarze et al. Mol Biol Evol. 2014 Oct.

Abstract

Agnathans (jawless vertebrates) occupy a key phylogenetic position for illuminating the evolution of vertebrate anatomy and physiology. Evaluation of the agnathan globin gene repertoire can thus aid efforts to reconstruct the origin and evolution of the globin genes of vertebrates, a superfamily that includes the well-known model proteins hemoglobin and myoglobin. Here, we report a comprehensive analysis of the genome of the sea lamprey (Petromyzon marinus) which revealed 23 intact globin genes and two hemoglobin pseudogenes. Analyses of the genome of the Arctic lamprey (Lethenteron camtschaticum) identified 18 full length and five partial globin gene sequences. The majority of the globin genes in both lamprey species correspond to the known agnathan hemoglobins. Both genomes harbor two copies of globin X, an ancient globin gene that has a broad phylogenetic distribution in the animal kingdom. Surprisingly, we found no evidence for an ortholog of neuroglobin in the lamprey genomes. Expression and phylogenetic analyses identified an ortholog of cytoglobin in the lampreys; in fact, our results indicate that cytoglobin is the only orthologous vertebrate-specific globin that has been retained in both gnathostomes and agnathans. Notably, we also found two globins that are highly expressed in the heart of P. marinus, thus representing functional myoglobins. Both genes have orthologs in L. camtschaticum. Phylogenetic analyses indicate that these heart-expressed globins are not orthologous to the myoglobins of jawed vertebrates (Gnathostomata), but originated independently within the agnathans. The agnathan myoglobin and hemoglobin proteins form a monophyletic group to the exclusion of functionally analogous myoglobins and hemoglobins of gnathostomes, indicating that specialized respiratory proteins for O2 transport in the blood and O2 storage in the striated muscles evolved independently in both lineages. This dual convergence of O2-transport and O2-storage proteins in agnathans and gnathostomes involved the convergent co-option of different precursor proteins in the ancestral globin repertoire of vertebrates.

Keywords: Agnatha; convergent evolution; cytoglobin; gene duplication; hemoglobin; myoglobin.

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Figures

F<sc>ig</sc>. 1.
Fig. 1.
Alignment of 23 sea lamprey globin proteins with human myoglobin (MB) and α-hemoglobin (HbA1). Incomplete sea lamprey sequences are not shown. The α-helical structure of sea lamprey aHb5 is shown on top of the alignments. Amino acids strictly conserved between the globins are shaded (black: 100% conservation, dark gray: 80%, light gray: 60%). The functionally important phenylalanine (F) at CD1 and the distal and proximal histidines (H) at E7 and E8 are indicated. The globin consensus numbering is given below the sequences.
F<sc>ig</sc>. 2.
Fig. 2.
Simplified Bayesian phylogenetic tree of agnathan globins. The numbers at the nodes are posterior probabilities. The bar represents 0.4 PAM distance. Sea lamprey globins are colored in red, Arctic lamprey globins are blue. The common names of the species are given. See supplementary table S1, Supplementary Material online, for details of the proteins and supplementary figure S3, Supplementary Material online, for the full version of the tree.
F<sc>ig</sc>. 3.
Fig. 3.
Synteny analyses of selected lamprey globin genes. Orthologous genes are shown in the same color. (A) The genes NPRL3, RAB40, and WDR90 link the aHb cluster on scaffold KE993782 with the gnathostome αHb cluster. (B) FOXK2 and RAB40 paralogs (hatched) link the Arctic lamprey Cygb-scaffold (KE993827) with the gnathostome Cygb locus, whereas RNF157, FOXJ1 and EXOC7 link this latter scaffold to aMb1–aHb6 cluster (scaffold KE993736).
F<sc>ig</sc>. 4.
Fig. 4.
Quantification of mRNA levels of selected sea lamprey globins in different tissues. Using qRT-PCR the mRNA copy numbers of the aMb1 (A) and Mb2 (B), the putative Cygb (C), and aHb5a (D) were obtained. aMb1 and aMb2 were detected in heart, brain, gill, and skeletal muscle, aHb5a was most highly expressed in blood, whereas Cygb showed a widespread distribution.
F<sc>ig</sc>. 5.
Fig. 5.
ISH of sea lamprey aHb5a (A, E) and aMb1 (C, G) antisense RNA probes in heart (A, C) and muscle (E, G) cryosections. aHb5a mRNA was detected in erythrocytes (A), which reside in the blood vessels, but not in the muscle tissue (E). Expression of aMb1 mRNA was detected as diffuse staining in heart sections (C) and in myonucleus of myofibers in muscle (G). Sense probes, which were used as negative controls, showed no signals (B, D, F, H). Scale bar = 100 µm.
F<sc>ig</sc>. 6.
Fig. 6.
Hypothesized evolution of respiratory function in vertebrate globins. The three possible positions of Cygb are depicted in simplified models illustrating alternative relationships among the eight primary vertebrate globin types (A–C). One bar indicates the origin of O2-storage function (and, possibly, pentacoordination), whereas two bars indicate the origin of blood O2-tansport function. The circle indicates the last common ancestor of the vertebrate-specific globins and the arrow the time of divergence of Agnatha and Gnathostomata. Note that if last common ancestor of the vertebrate-specific globins already had an O2-storage function, this function may have also been lost in Cygb.
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