Found and Lost: The Fates of Horizontally Acquired Genes in Arthropod-SymbioticSpiroplasma

Abstract

Horizontal gene transfer (HGT) is an important mechanism that contributed to biological diversity, particularly in bacteria. Through acquisition of novel genes, the recipient cell may change its ecological preference and the process could promote speciation. In this study, we determined the complete genome sequence of two Spiroplasma species for comparative analyses and inferred the putative gene gains and losses. Although most Spiroplasma species are symbionts of terrestrial insects, Spiroplasma eriocheiris has evolved to be a lethal pathogen of freshwater crustaceans. We found that approximately 7% of the genes in this genome may have originated from HGT and these genes expanded the metabolic capacity of this organism. Through comparison with the closely related Spiroplasma atrichopogonis, as well as other more divergent lineages, our results indicated that these HGT events could be traced back to the most recent common ancestor of these two species. However, most of these horizontally acquired genes have been pseudogenized in S. atrichopogonis, suggesting that they did not contribute to the fitness of this lineage that maintained the association with terrestrial insects. Thus, accumulation of small deletions that disrupted these foreign genes was not countered by natural selection. On the other hand, the long-term survival of these horizontally acquired genes in the S. eriocheiris genome hinted that they might play a role in the ecological shift of this species. Finally, the implications of these findings and the conflicts among gene content, 16S rRNA gene sequencing, and serological typing, are discussed in light of defining bacterial species.

Winding paths to simplicity: genome evolution in facultative insect symbionts

“…apis indicated horizontal gene acquisition from divergent sources, but the functional significance is unclear (Ku et al. 2014; Lo, Gasparich and Kuo 2015). …”

“…Among the cases of inferred horizontal gene acquisitions in Spiroplasma , the major sources appear to be those from within the class Mollicutes and share this alternative code (Chang et al. 2014; Lo, Gasparich and Kuo 2015). However, this observation may be explained by their shared ecological niches and codon usage biases, such that gene transfers are facilitated by frequent contacts and possibly higher chances of persistence.…”

“…Compared to the viral invasion found in the Citri clade and the stasis found in the Chrysopicola clade, the genome evolution in the Mirum clade is dominated by massive gains (and losses) of horizontally transferred genes (Lo, Gasparich and Kuo 2015). While most described Spiroplasma species are associated with terrestrial insects, Sp.…”

“…The Sp. eriocheiris genome analysis suggests that ∼7% of its CDSs may have been acquired from lineages outside of Spiroplasma and these foreign genes expanded its metabolic capacity (Lo, Gasparich and Kuo 2015). Interestingly, examination of its sister species Sp.…”

“…After the divergence, Sp. atrichopogonis has acquired several transposon-like segments, possibly from Citri-clade donors, indicating frequent genetic exchange between symbionts sharing similar niches, particularly for symbionts with close phylogenetic relationships (Lo, Gasparich and Kuo 2015). …”