A reversible mutation in a genomic hotspot saves bacterial swarms from extinction

Idan Hefetz; Ofir Israeli; Gal Bilinsky; Inbar Plaschkes; Einat Hazkani-Covo; Zvi Hayouka; Adam Lampert; Yael Helman

doi:10.1016/j.isci.2023.106043

A reversible mutation in a genomic hotspot saves bacterial swarms from extinction

iScience. 2023 Jan 25;26(2):106043. doi: 10.1016/j.isci.2023.106043. eCollection 2023 Feb 17.

Authors

Idan Hefetz^{1

2}, Ofir Israeli³, Gal Bilinsky³, Inbar Plaschkes⁴, Einat Hazkani-Covo⁵, Zvi Hayouka⁶, Adam Lampert⁷, Yael Helman²

Affiliations

¹ Department of Biotechnology, Institute for Biological Research, Ness-Ziona, Israel.
² Department of Plant Pathology and Microbiology, IES, Robert H. Smith Faculty of Agriculture, Food and Environment, The Hebrew University of Jerusalem, Rehovot, Israel.
³ Department of Biochemistry and Molecular Biology, Institute for Biological Research, Ness-Ziona, Israel.
⁴ Info-CORE, Bioinformatics Unit of the I-CORE at the Hebrew University of Jerusalem, Jerusalem, Israel.
⁵ Department of Natural and Life Sciences, The Open University of Israel, Ra'anana, Israel.
⁶ Department of Biochemistry, Robert H. Smith Faculty of Agriculture, Food and Environment, The Hebrew University of Jerusalem, Rehovot, Israel.
⁷ Institute of Environmental Sciences (IES), Robert H. Smith Faculty of Agriculture, Food and Environment, The Hebrew University of Jerusalem, Rehovot, Israel.

Abstract

Microbial adaptation to changing environmental conditions is frequently mediated by hypermutable sequences. Here we demonstrate that such a hypermutable hotspot within a gene encoding a flagellar unit of Paenibacillus glucanolyticus generated spontaneous non-swarming mutants with increased stress resistance. These mutants, which survived conditions that eliminated wild-type cultures, could be carried by their swarming siblings when the colony spread, consequently increasing their numbers at the spreading edge. Of interest, the hypermutable nature of the aforementioned sequence enabled the non-swarming mutants to serve as "seeds" for a new generation of wild-type cells through reversion of the mutation. Using a mathematical model, we examined the survival dynamics of P. glucanolyticus colonies under fluctuating environments. Our experimental and theoretical results suggest that the non-swarming, stress-resistant mutants can save the colony from extinction. Notably, we identified this hypermutable sequence in flagellar genes of additional Paenibacillus species, suggesting that this phenomenon could be wide-spread and ecologically important.

Keywords: Biological sciences; Genetics; Mathematical biosciences; Microbiology.