Single mutation makes Escherichia coli an insect mutualist

Ryuichi Koga, Minoru Moriyama, Naoko Onodera-Tanifuji, Yoshiko Ishii, Hiroki Takai, Masaki Mizutani, Kohei Oguchi, Reiko Okura, Shingo Suzuki, Yasuhiro Gotoh, Tetsuya Hayashi, Masahide Seki, Yutaka Suzuki, Yudai Nishide, Takahiro Hosokawa, Yuichi Wakamoto, Chikara Furusawa, Takema Fukatsu

Research output: Contribution to journalArticlepeer-review

4 Citations (Scopus)

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.

Original languageEnglish
Pages (from-to)1141-1150
Number of pages10
JournalNature Microbiology
Volume7
Issue number8
DOIs
Publication statusPublished - Aug 2022

All Science Journal Classification (ASJC) codes

  • Microbiology
  • Immunology
  • Applied Microbiology and Biotechnology
  • Genetics
  • Microbiology (medical)
  • Cell Biology

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