Abstract
Nutritional symbioses between bacteria and insects are prevalent and diverse, allowing insects to expand their feeding strategies and niches. A common consequence of long-term associations is a considerable reduction in symbiont genome size likely influenced by the radical shift in selective pressures as a result of the less variable environment within the host. While several of these cases can be found across distinct insect species, most examples provide a limited view of a single or few stages of the process of genome reduction. Stink bugs (Pentatomidae) contain inherited gamma-proteobacterial symbionts in a modified organ in their midgut and are an example of a long-term nutritional symbiosis, but multiple cases of new symbiont acquisition throughout the history of the family have been described. We sequenced the genomes of 11 symbionts of stink bugs with sizes that ranged from equal to those of their free-living relatives to less than 20%. Comparative genomics of these and previously sequenced symbionts revealed initial stages of genome reduction including an initial pseudogenization before genome reduction, followed by multiple stages of progressive degeneration of existing metabolic pathways likely to impact host interactions such as cell wall component biosynthesis. Amino acid biosynthesis pathways were retained in a similar manner as in other nutritional symbionts. Stink bug symbionts display convergent genome reduction events showing progressive changes from a free-living bacterium to a host-dependent symbiont. This system can therefore be used to study convergent genome evolution of symbiosis at a scale not previously available.
Highlights
Nutritional symbioses between bacteria and insects are prevalent and diverse, allowing insects to expand their feeding strategies and niches
We are confident that the genomes described represent the complete gene set for each symbiont with few and negligible omissions given that: 1) the assemblies contained no additional contigs of similar or higher coverage, 2) the evidence that each contig was connected to the main component via the ribosomal gene operon which is present multiple times in each genome, 3) the multiple assemblies for symbionts of the Edessa matched in contig number and connections to the repetitive sequences, and 4) in the case of the unreduced genomes, the Benchmarking Universal Single Copy Orthologs (BUSCO) completeness was above 96%
Genome reduction has been widely studied across insect symbionts, yet comparative genomic methods studying convergence in genome evolution have been limited to either too distant or too similar instances of symbiosis
Summary
Nutritional symbioses between bacteria and insects are prevalent and diverse, allowing insects to expand their feeding strategies and niches. We sequenced the genomes of 11 symbionts of stink bugs with sizes that ranged from equal to those of their free-living relatives to less than 20% Comparative genomics of these and previously sequenced symbionts revealed initial stages of genome reduction including an initial pseudogenization before genome reduction, followed by multiple stages of progressive degeneration of existing metabolic pathways likely to impact host interactions such as cell wall component biosynthesis. Members of the Pentatomomorpha often harbor an extracellular bacterial symbiont within posterior midgut crypts[17,18,19] While this symbiotic organ is fairly similar across a wide variety of families, other traits of the symbiosis can be quite variable, including the acquisition strategy[17,20,21,22,23], degree of cophylogeny between host and symbiont[24], and the symbiont’s reliance on its host[17]. The most common scenario is that of more specific host-symbiont associations, where a single host species is consistently associated with a single symbiont[24,28,29,30,31], and cophylogeny is detected between g enera[29,32,33] but not necessarily at higher taxonomic levels[34,35], which would indicate multiple associations at different points in time throughout the family
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