Three globin lineages belonging to two structural classes in genomes from the three kingdoms of life

Abstract

Although most globins, including the N-terminal domains within chimeric proteins such as flavohemoglobins and globin-coupled sensors, exhibit a 3/3 helical sandwich structure, many bacterial, plant, and ciliate globins have a 2/2 helical sandwich structure. We carried out a comprehensive survey of globins in the genomes from the three kingdoms of life. Bayesian phylogenetic trees based on manually aligned sequences indicate the possibility of past horizontal globin gene transfers from bacteria to eukaryotes. blastp searches revealed the presence of 3/3 single-domain globins related to the globin domains of the bacterial and fungal flavohemoglobins in many bacteria, a red alga, and a diatom. Iterated psi-blast searches based on groups of globin sequences found that only the single-domain globins and flavohemoglobins recognize the eukaryote 3/3 globins, including vertebrate neuroglobins, alpha- and beta-globins, and cytoglobins. The 2/2 globins recognize the flavohemoglobins, as do the globin coupled sensors and the closely related single-domain protoglobins. However, the 2/2 globins and the globin-coupled sensors do not recognize each other. Thus, all globins appear to be distributed among three lineages: (i) the 3/3 plant and metazoan globins, single-domain globins, and flavohemoglobins; (ii) the bacterial 3/3 globin-coupled sensors and protoglobins; and (iii) the bacterial, plant, and ciliate 2/2 globins. The three lineages may have evolved from an ancestral 3/3 or 2/2 globin. Furthermore, it appears likely that the predominant functions of globins are enzymatic and that oxygen transport is a specialized development that accompanied the evolution of metazoans.

Fig. 1.

A consensus phylogenetic tree of major globin groups from the three kingdoms of life. The detailed version and the alignment are provided in Figs. 9 and 10, respectively.

Fig. 2.

A diagrammatic representation of the time scale of life based on refs. –, depicting the distribution of the three globin lineages in the three kingdoms of life. The origin of Cyanobacteria (Cy) is estimated at ≈2,600 Mya, and the divergence of plants (Pl), animals (An), and fungi (Fu) is estimated at ≈1,500 Mya. The red arrows indicate the two generally accepted endosymbiotic events: between an α-proteobacterium (Ap) and a eukaryote at ≈1,800 Mya, resulting in the emergence of mitochondria (M), and between a cyanobacterium and a eukaryote at ≈1,500 Mya, resulting in the formation of plastids (P). The dotted lines indicate uncertainty in dating the split. Aq, Aquificales; OB, other bacteria; Al, Algae; Em, Embryophytes (land plants); OEk, other eukaryotes; Cr, Crenarcheota; Eu, Euryacheota.