Abstract
Intracellular thioautotrophic symbionts of deep-sea vesicomyid clams lack some DNA repair genes and are thought to be undergoing reductive genome evolution (RGE). In this study, we addressed two questions, 1) how these symbionts lost their DNA repair genes and 2) how such losses affect RGE. For the first question, we examined genes associated with nucleotide excision repair (NER; uvrA, uvrB, uvrC, uvrD, uvrD paralog [uvrDp] and mfd) in 12 symbionts of vesicomyid clams belonging to two clades (5 clade I and 7 clade II symbionts). While uvrA, uvrDp and mfd were conserved in all symbionts, uvrB and uvrC were degraded in all clade I symbionts but were apparently intact in clade II symbionts. UvrD was disrupted in two clade II symbionts. Among the intact genes in Ca. Vesicomyosocius okutanii (clade I), expressions of uvrD and mfd were detected by reverse transcription-polymerase chain reaction (RT-PCR), but those of uvrA and uvrDp were not. In contrast, all intact genes were expressed in the symbiont of Calyptogena pacifica (clade II). To assess how gene losses affect RGE (question 2), genetic distances of the examined genes in symbionts from Bathymodiolus septemdierum were shown to be larger in clade I than clade II symbionts. In addition, these genes had lower guanine+cytosine (GC) content and higher repeat sequence densities in clade I than measured in clade II. Our results suggest that NER genes are currently being lost from the extant lineages of vesicomyid clam symbionts. The loss of NER genes and mutY in these symbionts is likely to promote increases in genetic distance and repeat sequence density as well as reduced GC content in genomic genes, and may have facilitated reductive evolution of the genome.
Highlights
Vesicomyid clams, commonly found in large, dense aggregations at deep-sea methane seeps and hydrothermal vents [1, 2] have single thioautotrophic gammaproteobacterial symbionts in their gill epithelial cells
Consensus helicase motifs of bacterial UvrBs were mostly found in the coded amino acid sequences of the intact uvrBs in clade II (Figs 1 and S2), suggesting that they were functional
In clade I symbionts uvrB was degraded and its deletion pattern differed among symbionts, except for a nearly identical pattern for the symbionts of 2 sibling species, P. soyoae and P. kilmeri (Figs 1 and S2)
Summary
Vesicomyid clams, commonly found in large, dense aggregations at deep-sea methane seeps and hydrothermal vents [1, 2] have single thioautotrophic gammaproteobacterial symbionts in their gill epithelial cells. Reconstruction of phylogenies using ribosomal RNA sequences indicates that the symbionts of vesicomyids comprise two phylogenetic clades (clade I and II) [3]. Genome sequences of symbionts are known from 2 vesicomyid species, Phreagena (formerly Calyptogena) okutanii (Ca. Vesicomyosocius okutanii, Vok, clade I) and Calyptogena magnifica (Ca. Ruthia magnifica, Rma, clade II), with sizes of 1.02 and 1.16 Mb, respectively [4, 5]. Comparative genome analysis has shown that their genomes are in an active phase of reductive genome evolution (RGE) [3, 6]
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