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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.

SUBMITTER: Koga R

PROVIDER: S-EPMC9352592 | biostudies-literature | 2022 Aug

REPOSITORIES: biostudies-literature

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Single mutation makes Escherichia coli an insect mutualist.

Koga Ryuichi R Moriyama Minoru M Onodera-Tanifuji Naoko N Ishii Yoshiko Y Takai Hiroki H Mizutani Masaki M Oguchi Kohei K Okura Reiko R Suzuki Shingo S Gotoh Yasuhiro Y Hayashi Tetsuya T Seki Masahide M Suzuki Yutaka Y Nishide Yudai Y Hosokawa Takahiro T Wakamoto Yuichi Y Furusawa Chikara C Fukatsu Takema T

Nature microbiology 20220804 8

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 n ...[more]

PMID: 35927448

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Project description:Although glutathione (GSH) has been shown to influence the antimicrobial effects of many kinds of antibiotics, little is known about its role in relation to trimethoprim (TMP), a widely used antifolate. In this study, several genes related to glutathione metabolism were deleted in different Escherichia coli strains (i.e., O157:H7 and ATCC 25922), and their effects on susceptibility to TMP were tested. The results showed that deleting gshA, gshB, grxA, and cydD caused TMP resistance, and deleting cydD also caused resistance to other drugs. Meanwhile, deleting gshA, grxA, and cydD resulted in a significant decrease of the periplasmic glutathione content. Supplementing exogenous GSH or further deleting glutathione importer genes (gsiB and ggt) restored TMP sensitivity to ΔcydD. Subsequently, the results of quantitative-reverse transcription PCR experiments showed that expression levels of acrA, acrB, and tolC were significantly upregulated in both ΔgrxA and ΔcydD. Correspondingly, deleting cydD led to a decreased accumulation of TMP within bacterial cells, and further deleting acrA, acrB, or tolC restored TMP sensitivity to ΔcydD. Inactivation of CpxR and SoxS, two transcriptional factors that modulate the transcription of acrAB-tolC, restored TMP sensitivity to ΔcydD. Furthermore, mutations of gshA, gshB, grxA, cydC, and cydD are highly prevalent in E. coli clinical strains. Collectively, these data suggest that reducing the periplasmic glutathione content of E. coli leads to increased expression of acrAB-tolC with the involvement of CpxR and SoxS, ultimately causing drug resistance. To the best of our knowledge, this is the first report showing a linkage between periplasmic GSH and drug resistance in bacteria. IMPORTANCE After being used extensively for decades, trimethoprim still remains one of the key accessible antimicrobials recommended by the World Health Organization. A better understanding of the mechanisms of resistance would be beneficial for the future utilization of this drug. It has been shown that the AcrAB-TolC efflux pump is associated with trimethoprim resistance in E. coli clinical strains. In this study, we show that E. coli can sense the periplasmic glutathione content with the involvement of the CpxAR two-component system. As a result, reducing the periplasmic glutathione content leads to increased expression of acrA, acrB, and tolC via CpxR and SoxS, causing resistance to antimicrobials, including trimethoprim. Meanwhile, mutations in the genes responsible for periplasmic glutathione content maintenance are highly prevalent in E. coli clinical isolates, indicating a potential correlation of the periplasmic glutathione content and clinical antimicrobial resistance, which merits further investigation.

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Single mutation makes Escherichia coli an insect mutualist.

Publications

Single mutation makes Escherichia coli an insect mutualist.

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