Romero F and Nishigaki T (2019), Comparative genomic analysis suggests that the ...

ECB-ART-47355

Zoological Lett 2019 Jan 01;5:25. doi: 10.1186/s40851-019-0141-3.

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Comparative genomic analysis suggests that the sperm-specific sodium/proton exchanger and soluble adenylyl cyclase are key regulators of CatSper among the Metazoa.

Romero F , Nishigaki T .

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Background: CatSper is a sperm-specific calcium ion (Ca2+) channel, which regulates sperm flagellar beating by tuning cytoplasmic Ca2+ concentrations. Although this Ca2+ channel is essential for mammalian fertilization, recent bioinformatics analyses have revealed that genes encoding CatSper are heterogeneously distributed throughout the eukaryotes, including vertebrates. As this channel is activated by cytoplasmic alkalization in mammals and sea urchins, it has been proposed that the sperm-specific Na+/H+ exchanger (sNHE, a product of the SLC9C gene family) positively regulates its activity. In mouse, sNHE is functionally coupled to soluble adenylyl cyclase (sAC). CatSper, sNHE, and sAC have thus been considered functionally interconnected in the control of sperm motility, at least in mouse and sea urchin. Results: We carried out a comparative genomic analysis to explore phylogenetic relationships among CatSper, sNHE and sAC in eukaryotes. We found that sNHE occurs only in Metazoa, although sAC occurs widely across eukaryotes. In animals, we found correlated and restricted distribution patterns of the three proteins, suggesting coevolution among them in the Metazoa. Namely, nearly all species in which CatSper is conserved also preserve sNHE and sAC. In contrast, in species without sAC, neither CatSper nor sNHE is conserved. On the other hand, the distribution of another testis-specific NHE (NHA, a product of the SLC9B gene family) does not show any apparent association with that of CatSper. Conclusions: Our results suggest that CatSper, sNHE and sAC form prototypical machinery that functions in regulating sperm flagellar beating in Metazoa. In non-metazoan species, CatSper may be regulated by other H+ transporters, or its activity might be independent of cytoplasmic pH.

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Species referenced: Echinodermata
Genes referenced: adcy10 LOC100887844 spata18 srpl

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	Fig. 1. Distribution of genes encoding CatSper, sNHE, and sAC in the entire phylogenetic tree of eukaryotes. The tree indicates the metazoan taxonomic groups (green background) and non-metazoan species (purple background). Closed boxes represent the presence of genes encoding each protein: CatSper (black), sNHE (blue) and sAC (red). Taxonomic groups with open boxes have varied gene distributions within the groups (the detailed distributions can be seen in the following figures). Homologues for sNHE and sAC are represented as half-filled boxes, blue and red, respectively. The phylogenetic tree was prepared based on the Tree of Life Web project (http://www.tolweb.org/tree/) with some modifications based on recent reports [93–96]. The branching patterns do not represent the proportional evolutionary rate
	Fig. 2. Distribution of genes encoding CatSper and sAC in birds. Only two species belonging to the Palaeognathae show conservation of genes encoding CatSper (black boxes), and no birds show conservation of sNHE. In some species, full or truncated isoforms of sAC (red box) are conserved. Species marked with an asterisk possess a pseudogene for the sAC (Fig. 5C). This phylogenetic tree was prepared based on a recent phylogenetic study of birds [97]. The branching patterns do not represent the proportional evolutionary rate
	Fig. 3. Distribution of genes encoding the three proteins in 12 species of ray-finned fishes. Boxes represent the presence of genes as shown in Fig. 1. The phylogenetic tree was prepared based on a recent phylogenetic study of this taxon [93]. The branching patterns do not represent the proportional evolutionary rate
	Fig. 4. Distribution of genes encoding the three proteins in the Arthropoda. Boxes represent the presence of genes as shown in Fig. 1. The phylogenetic tree was prepared based on the Tree of Life Web project (http://www.tolweb.org/tree/). The branching patterns do not represent the proportional evolutionary rate
	Fig. 5. Shared synteny for SLC9C and pseudogenization of SLC9C and ADCY10. A. The upper panel shows synteny block comparisons around SLC9C among lizard, coelacanth, spotted gar, and white-throated tinamou. The lower panel shows an alignment of representative protein fragments of sNHE from lizard, coelacanth, spotted gar and the deduced amino acid sequence of a predicted exon obtained from white-throated tinamou (PE of Tinamu). B. The upper panel shows synteny block comparisons around SLC9C among postman butterfly, monarch butterfly and fruit fly. The lower panel shows an alignment of representative protein fragments of sNHE from the two butterflies (bf) and the deduced amino acid sequence of a predicted exon obtained from the fruit fly (PE of Fly). C. An alignment of representative protein fragments of sAC from lizard, chicken and white-throated tinamou (Tinamu) and the deduced amino acid sequences of three PE obtained from the turkey, duck, and pigeon. In synteny blocks, the arrangement reflects the order and orientation of genes in each indicated chromosome. In the case of the white-throated tinamou, the name of the unplaced genomic scaffold is indicated instead of the chromosome number. Chromosomes (Chr) are not represented to the scale of base-pair length. In all alignments, coloured highlights indicate ≥50% conserved (blue) and similar (pink) amino acid. Abbreviations for orthologues are listed in Table S2
	Fig. 6. Synteny block comparison of SLC9B (NHA) and distribution of genes encoding CatSper, sNHE and sAC in vertebrates. Synteny blocks around SLC9B1 (NHA1) and SLC9B2 (NHA2) among human, chicken, frog, medaka, zebrafish, and lizard are shown together with distributions of genes encoding CatSper (black), sNHE (blue) and sAC (red). In synteny blocks, the arrangement reflects the order and orientation of genes in each chromosome. Chromosomes (Chr) are not represented to the scale of base-pair length

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