Genome Degeneration and Adaptation in a Nascent Stage of Symbiosis

Abstract

Symbiotic associations between animals and microbes are ubiquitous in nature, with an estimated 15% of all insect species harboring intracellular bacterial symbionts. Most bacterial symbionts share many genomic features including small genomes, nucleotide composition bias, high coding density, and a paucity of mobile DNA, consistent with long-term host association. In this study, we focus on the early stages of genome degeneration in a recently derived insect-bacterial mutualistic intracellular association. We present the complete genome sequence and annotation of Sitophilus oryzae primary endosymbiont (SOPE). We also present the finished genome sequence and annotation of strain HS, a close free-living relative of SOPE and other insect symbionts of the Sodalis-allied clade, whose gene inventory is expected to closely resemble the putative ancestor of this group. Structural, functional, and evolutionary analyses indicate that SOPE has undergone extensive adaptation toward an insect-associated lifestyle in a very short time period. The genome of SOPE is large in size when compared with many ancient bacterial symbionts; however, almost half of the protein-coding genes in SOPE are pseudogenes. There is also evidence for relaxed selection on the remaining intact protein-coding genes. Comparative analyses of the whole-genome sequence of strain HS and SOPE highlight numerous genomic rearrangements, duplications, and deletions facilitated by a recent expansion of insertions sequence elements, some of which appear to have catalyzed adaptive changes. Functional metabolic predictions suggest that SOPE has lost the ability to synthesize several essential amino acids and vitamins. Analyses of the bacterial cell envelope and genes encoding secretion systems suggest that these structures and elements have become simplified in the transition to a mutualistic association.

Insights into the metabolism, lifestyle and putative evolutionary history of the novel archaeal phylum ‘Diapherotrites’

“…Many of the genomic streamlining features observed in Cand. IA genome, such as small genome size, small intergenic regions, low incidences of gene duplication and low number of rRNA operons, have been associated with specific trophic lifestyles, mainly oligotrophy and obligate symbiosis (Giovannoni et al, 2005;Lauro et al, 2009;Walker et al, 2010;Grote et al, 2012;Swan et al, 2013), where they appear to be a reflection of the accessibility of nutrients, as well as the occurrence of genetic drift in obligate symbionts (Mira et al, 2001;Wernegreen, 2002;Giovannoni et al, 2005;Oakeson et al, 2014). However, detailed comparative analysis of the metabolism and genomic features of Cand.…”

Repeated replacement of an intrabacterial symbiont in the tripartite nested mealybug symbiosis

“…Genome size is strongly correlated to endosymbiotic age in bacteria, especially at the onset of symbiosis, when genome reduction can be rapid (53)(54)(55)(56)(57). Most relevant to our argument here is the speed with which genome reduction has been shown to take place in Sodalisallied bacteria closely related to the γ-proteobacterial symbionts of mealybugs (34,58,59). It has been estimated that as much as 55% of an ancestral Sodalis genome was lost on the transition to endosymbiosis in a mere ∼28,000 y, barely enough time for 1% sequence divergence to accumulate between the new symbiont and a free-living relative (58).…”

Small genome symbiont underlies cuticle hardness in beetles

“…Considering that many bacteria are capable of synthesizing amino acids including tyrosine, any bacterial infections with secondary facultative symbionts or gut microbial associates may potentially result in complementation of Nardonella's biological function. Such a symbiont replacement has been presumed and best documented for grain weevils of the genus Sitophilus, in which Nardonella was replaced by a γ-proteobacterial lineage Sodalis pierantonius (23,24,32,50). The weevil-associated Sodalis genome was determined as 4.5 Mb in size, which was much larger than the Nardonella genome and retaining many metabolic pathways intact; however, the Sodalis genome was full of amplified IS elements and pseudogenes (50,51), representing an early stage of the degenerative genome evolution after replacing the original Nardonella symbiont.…”

“…Such a symbiont replacement has been presumed and best documented for grain weevils of the genus Sitophilus, in which Nardonella was replaced by a γ-proteobacterial lineage Sodalis pierantonius (23,24,32,50). The weevil-associated Sodalis genome was determined as 4.5 Mb in size, which was much larger than the Nardonella genome and retaining many metabolic pathways intact; however, the Sodalis genome was full of amplified IS elements and pseudogenes (50,51), representing an early stage of the degenerative genome evolution after replacing the original Nardonella symbiont. A number of classic and recent studies have documented a variety of biological roles of the Sodalis symbiont for the grain weevils: at phenotypic levels, enhanced growth, survival, and fecundity (37,52,53), improved flight activity (52,54) and facilitated cuticular tanning and hardening (36,37,52); and at biochemical and metabolic levels, provisioning of B vitamins such as pantothenic acid, biotin, and riboflavin (55), supply of aromatic amino acids phenylalanine and tyrosine (36,37), metabolism of methionine and sarcosine (56,57), and involvement in mitochondrial energy metabolism (58,59).…”