Abstract

Genome reduction is a recurring theme of symbiont evolution. The genus Spiroplasma contains species that are mostly facultative insect symbionts. The typical genome sizes of those species within the Apis clade were estimated to be ∼1.0–1.4 Mb. Intriguingly, Spiroplasma clarkii was found to have a genome size that is >30% larger than the median of other species within the same clade. To investigate the molecular evolution events that led to the genome expansion of this bacterium, we determined its complete genome sequence and inferred the evolutionary origin of each protein-coding gene based on the phylogenetic distribution of homologs. Among the 1,346 annotated protein-coding genes, 641 were originated from within the Apis clade while 233 were putatively acquired from outside of the clade (including 91 high-confidence candidates). Additionally, 472 were specific to S. clarkii without homologs in the current database (i.e., the origins remained unknown). The acquisition of protein-coding genes, rather than mobile genetic elements, appeared to be a major contributing factor of genome expansion. Notably, >50% of the high-confidence acquired genes are related to carbohydrate transport and metabolism, suggesting that these acquired genes contributed to the expansion of both genome size and metabolic capability. The findings of this work provided an interesting case against the general evolutionary trend observed among symbiotic bacteria and further demonstrated the flexibility of Spiroplasma genomes. For future studies, investigation on the functional integration of these acquired genes, as well as the inference of their contribution to fitness could improve our knowledge of symbiont evolution.

Highlights

  • The patterns of genome evolution among diverse symbiotic bacteria are characterized by a general trend of genome reduction (Moran and Plague 2004; Ochman and Davalos 2006; Toft and Andersson 2010; McCutcheon and Moran 2012; Moran and Bennett 2014)

  • Examination of the chromosome organization and gene content revealed that the genome expansion was not attributed to the invasion of plectroviruses as those found within the Spiroplasma Citri clade, in which viral sequences account for 20% of the chromosome in extant species (Carle et al 2010; Alexeev et al 2012; Ku et al 2013; Lo, Chen, et al 2013; Paredes et al 2015)

  • These species-specific genes appear to be the main contributing factor of the genome expansion observed in S. clarkii. Some of these may be artifacts of gene prediction, we expect that a high proportion of these genes may be acquired genes without known donors. The reason for this inference is that all of these Spiroplasma genomes were annotated by our research group based on the same procedure and on average those species-specific genes account for only 16% of the total gene count in other Apis clade species

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Summary

Introduction

The patterns of genome evolution among diverse symbiotic bacteria are characterized by a general trend of genome reduction (Moran and Plague 2004; Ochman and Davalos 2006; Toft and Andersson 2010; McCutcheon and Moran 2012; Moran and Bennett 2014). The genus Spiroplasma within the class Mollicutes contains diverse species that are mostly facultative insect symbionts capable of horizontal transmission (Gasparich et al 2004; Regassa and Gasparich 2006; Gasparich 2010). In recent years, these bacteria have been developed into a model system for the study of symbionts (Anbutsu and Fukatsu 2011; Bolan~os et al 2015; Lo et al 2016). To investigate the evolutionary processes and the genetic changes that led to the genome expansion in this bacterium, we determined the complete genome sequence of S. clarkii for comparative analysis

Materials and Methods
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Literature Cited

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