Testing the Domino Theory of Gene Loss in Buchnera aphidicola: The Relevance of Epistatic Interactions

Abstract

The domino theory of gene loss states that when some particular gene loses its function and cripples a cellular function, selection will relax in all functionally related genes, which may allow for the non-functionalization and loss of these genes. Here we study the role of epistasis in determining the pattern of gene losses in a set of genes participating in cell envelope biogenesis in the endosymbiotic bacteria Buchnera aphidicola. We provide statistical evidence indicating pairs of genes in B. aphidicola showing correlated gene loss tend to have orthologs in Escherichia coli known to have alleviating epistasis. In contrast, pairs of genes in B. aphidicola not showing correlated gene loss tend to have orthologs in E. coli known to have aggravating epistasis. These results suggest that during the process of genome reduction in B. aphidicola by gene loss, positive or alleviating epistasis facilitates correlated gene losses while negative or aggravating epistasis impairs correlated gene losses. We interpret this as evidence that the reduced proteome of B. aphidicola contains less pathway redundancy and more compensatory interactions, mimicking the situation of E. coli when grown under environmental constrains.

Enhanced Mutation Rate, Relaxed Selection, and the “Domino Effect” are associated with Gene Loss in Blattabacterium, A Cockroach Endosymbiont

“…Overall, our results provide support to the “domino-effect” theory, which posits that epistatic interactions among genes contribute to gene loss ( Dagan et al 2006 ; Martínez-Cano et al 2018 ). The clearest evidences of correlated gene loss were for genes composing metabolic pathways.…”

“…This phenomenon has been described repeatedly in species of insects associated with multiple endosymbiont species ( Moran and Bennett 2014 ; Douglas 2016 ; Sudakaran et al 2017 ). Finally, the “domino effect” hypothesis postulates that gene loss induces the loss of other dependent genes (e.g., within the same pathway) that are rendered nonfunctional ( Dagan et al 2006 ; Martínez-Cano et al 2018 ).…”

Comparative genomics of the primary endosymbiont Buchnera aphidicola in aphid hosts and their coevolutionary relationships

“…In total, the Buchnera aphidicola genomes range from 412 to 646 kb in length, thus comprising one of the smallest known cellular genomes of symbiotic bacteria [34,36,38,[41][42][43]. Buchnera has experienced drastic shrinkage in genome size, retaining only essential genes for its specialized lifestyle, and genome shrinkage may be ongoing [15,38,[44][45][46].…”