Winding paths to simplicity: genome evolution in facultative insect symbionts

Abstract

Symbiosis between organisms is an important driving force in evolution. Among the diverse relationships described, extensive progress has been made in insect–bacteria symbiosis, which improved our understanding of the genome evolution in host-associated bacteria. Particularly, investigations on several obligate mutualists have pushed the limits of what we know about the minimal genomes for sustaining cellular life. To bridge the gap between those obligate symbionts with extremely reduced genomes and their non-host-restricted ancestors, this review focuses on the recent progress in genome characterization of facultative insect symbionts. Notable cases representing various types and stages of host associations, including those from multiple genera in the family Enterobacteriaceae (class Gammaproteobacteria), Wolbachia (Alphaproteobacteria) and Spiroplasma (Mollicutes), are discussed. Although several general patterns of genome reduction associated with the adoption of symbiotic relationships could be identified, extensive variation was found among these facultative symbionts. These findings are incorporated into the established conceptual frameworks to develop a more detailed evolutionary model for the discussion of possible trajectories. In summary, transitions from facultative to obligate symbiosis do not appear to be a universal one-way street; switches between hosts and lifestyles (e.g. commensalism, parasitism or mutualism) occur frequently and could be facilitated by horizontal gene transfer.

Keywords: genome degradation; genome size; coding density; horizontal gene transfer; deletional bias; pseudogene; GC content; symbiosis; symbiotic bacteria; Arsenophonus; Hamiltonella; Regiella; Pantoea; Serratia; Sodalis; Spiroplasma; Wolbachia.

Figure 1.

Association between genome size and the number of CDSs in bacteria. Based on the 5043 complete genomes available from GenBank as of March 2016 and additional genomes listed in Table 1. Representative lineages are color-coded by the lifestyle.

Figure 2.

Functional classification of protein-coding genes. Functional category assignments are based on the COG database (Tatusov, Koonin and Lipman ; Tatusov et al.2003), the procedure of data analysis is based on that described in Lo et al. (2013a). Not all genomes listed in Table 1 are included for the following reasons: for closely related Spiroplasma species with nearly identical patterns, only few representatives are selected; for other genera, several draft genomes are omitted because the sequence records obtained from GenBank lack annotation of genes.

Figure 3.

A graphical summary of the genome evolution events in Spiroplasma and its derived lineages. Based on the results reported in the literature (Carle et al.; Thiaucourt et al.; Alexeev et al.; Ku et al.; Lo et al.,, ; Chang et al.; Ku et al.; Lo, Gasparich and Kuo ; Paredes et al.2015).

Figure 4.

Trajectories of genome size and coding density in symbiont evolution. During the process, one or more transitional events (e.g. strict host association, vertical transmission or endosymbiosis) could cause a sudden reduction in the effective population size and release a substantial proportion of genes from selective constraints. As a result, non-adaptive mutation accumulation could lead to large-scale gene inactivation, lowering the coding density. These pseudogenes would eventually be removed due to the mutational bias toward deletions commonly observed in bacterial genomes, leading to a higher coding density and a much smaller genome. In addition, small-scale events of genome degradation could occur continuously throughout the process. Importantly, not all symbionts would eventually develop obligate symbiosis and have extremely reduced genomes. Some may maintain facultative associations with their hosts and be commensals, parasites or mutualists. Transitions between symbiosis types and host switches may be possible by acquiring new genes through horizontal gene transfer or losing key genes through mutations.