Single mutation makes Escherichia coli an insect mutualist

Abstract

Microorganisms often live in symbiosis with their hosts, and some are considered mutualists, where all species involved benefit from the interaction. How free-living microorganisms have evolved to become mutualists is unclear. Here we report an experimental system in which non-symbiotic Escherichia coli evolves into an insect mutualist. The stinkbug Plautia stali is typically associated with its essential gut symbiont, Pantoea sp., which colonizes a specialized symbiotic organ. When sterilized newborn nymphs were infected with E. coli rather than Pantoea sp., only a few insects survived, in which E. coli exhibited specific localization to the symbiotic organ and vertical transmission to the offspring. Through transgenerational maintenance with P. stali, several hypermutating E. coli lines independently evolved to support the host’s high adult emergence and improved body colour; these were called ‘mutualistic’ E. coli. These mutants exhibited slower bacterial growth, smaller size, loss of flagellar motility and lack of an extracellular matrix. Transcriptomic and genomic analyses of ‘mutualistic’ E. coli lines revealed independent mutations that disrupted the carbon catabolite repression global transcriptional regulator system. Each mutation reproduced the mutualistic phenotypes when introduced into wild-type E. coli, confirming that single carbon catabolite repression mutations can make E. coli an insect mutualist. These findings provide an experimental system for future work on host–microbe symbioses and may explain why microbial mutualisms are omnipresent in nature.

Mechanisms Underpinning Morphogenesis of a Symbiotic Organ Specialized for Hosting an Indispensable Microbial Symbiont in Stinkbugs

“…In this study, we used a mass-reared laboratory strain of P. stali , which had been established from adult insects collected in Tsukuba, Ibaraki, Japan. Insect rearing was conducted essentially as described previously ( 16 , 19 , 46 ). In each plastic container (15 cm in diameter, 5 cm high), 10 to 20 adult insects were fed raw peanuts and distilled water (DW) containing 0.05% ascorbic acid (DWA), and allowed to lay eggs on filter paper placed inside the container.…”

Energy-harnessing problem solving of primordial life: Modeling the emergence of catalytic host-nested parasite life cycles

“…Intriguingly, ancient bacterial symbionts undergoing massive genome erosion repeatedly experienced extinction and replacement by pathogenic microbes [ 12 ]. Under experimental conditions the process of how free-living micro-organisms become symbionts is remarkably rapid and requires one single mutation [ 13 ]. Collectively, this suggests that evolution of life essentially is host-parasite coevolution [ 7 ].…”

At the threshold of symbiosis: the genome of obligately endosymbiotic ‘Candidatus Nebulobacter yamunensis’ is almost indistinguishable from that of a cultivable strain

“…While several closely related free-living/endosymbiotic microorganisms are known, the ‘Ca. Nebulobacter’ /Fastidiosibacter pair stands out as laying at the extreme end of the spectrum of examples, and highlights the sometimes-overlooked possibility that, at least in certain cases, the changes required to become an obligate endosymbiont may be very small [48], and perhaps yet unpredictable, despite the apparently cataclysmic nature of the resulting ecological change.…”