Abstract
Estimates suggest that at least half of all extant insect genera harbor obligate bacterial mutualists. Whereas an endosymbiotic relationship imparts many benefits upon host and symbiont alike, the intracellular lifestyle has profound effects on the bacterial genome. The obligate endosymbiont genome is a product of opposing forces: genes important to host survival are maintained through physiological constraint, contrasted by the fixation of deleterious mutations and genome erosion through random genetic drift. The obligate cockroach endosymbiont, Blattabacterium – providing nutritional augmentation to its host in the form of amino acid synthesis – displays radical genome alterations when compared to its most recent free-living relative Flavobacterium. To date, eight Blattabacterium genomes have been published, affording an unparalleled opportunity to examine the direction and magnitude of selective forces acting upon this group of symbionts. Here, we find that the Blattabacterium genome is experiencing a 10-fold increase in selection rate compared to Flavobacteria. Additionally, the proportion of selection events is largely negative in direction, with only a handful of loci exhibiting signatures of positive selection. These findings suggest that the Blattabacterium genome will continue to erode, potentially resulting in an endosymbiont with an even further reduced genome, as seen in other insect groups such as Hemiptera.
Highlights
Number of positive and negative selection events vs. individual COG size were carried out using Generalized Linear Models with Poisson distribution with number of selection sites as the response variable and total number of nucleotides in the genome associated with a specific COG as the explanatory variable
The number of positive selection events (F-value: 40.872, Df: 1, p-value: 6.16e-10, adjusted R-squared: 0.12) as well as negative selection events (F-value: 189.15, Df: 1, p-value: 2.2e-16, adjusted R-squared: 0.38) both showed strong positive correlation with gene length (Fig. 2a,c, respectively). This finding is consistent with the conclusions of previous studies, where natural selection is correlated with gene length[83]. Building upon this on a functional level, we noted that signatures of both positive and negative selection correlated strongly with the total number of nucleotides assigned to a specific COG across the Blattabacterium genome (Positive selection events: Chi-square p-value: 2.2e-16; Negative selection events: Chi-square p-value: 2.2e-16; Fig. 2b,d, respectively)
We find here that the overwhelming majority of mutations in the Blattabacterium genome are negative in direction, strongly suggesting that genome reduction is not driven by selective processes, but rather by random genetic drift; as has been suggested for numerous other obligate bacterial endosymbionts[32,35]
Summary
Number of positive and negative selection events vs. individual COG size were carried out using Generalized Linear Models with Poisson distribution with number of selection sites as the response variable and total number of nucleotides in the genome associated with a specific COG as the explanatory variable. As COG and gene length analyses used different datasets - number of selection events per total number of nucleotides of all genes associated with a given COG and number of selection events by gene length, respectively - we found that differing models better fit each type of analysis
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