Surfactin Facilitates Horizontal Gene Transfer in Bacillus subtilis.

Tjaša Danevčič,Iztok Dogsa,Polonca Stefanic,Mihael Spacapan,Ines Mandic-Mulec,Anna Dragoš,Anna Dragoš

doi:10.3389/fmicb.2021.657407

Abstract

Genetic competence for the uptake and integration of extracellular DNA is a key process in horizontal gene transfer (HGT), one of the most powerful forces driving the evolution of bacteria. In several species, development of genetic competence is coupled with cell lysis. Using Bacillus subtilis as a model bacterium, we studied the role of surfactin, a powerful biosurfactant and antimicrobial lipopeptide, in genetic transformation. We showed that surfactin itself promotes cell lysis and DNA release, thereby promoting HGT. These results, therefore, provide evidence for a fundamental mechanism involved in HGT and significantly increase our understanding of the spreading of antibiotic resistance genes and diversification of microbial communities in the environment.

Highlights

Surfactin is an important microbial surfactant with interesting biological activities
We provide evidence that DNA can be exchanged between strains without the external source of Extracellular DNA (eDNA) and that this horizontal gene transfer (HGT) is dependent on eDNA released through surfactin action
It has been shown that B. subtilis NCIB 3610 strain releases eDNA just before entry into the stationary phase and that the srfA mutant shows a defect in eDNA (Zafra et al, 2012), but the study did not indicate a direct role of surfactin in eDNA release

Summary

Introduction

Surfactin is an important microbial surfactant with interesting biological activities. In the Gram-positive bacterium Bacillus subtilis, the major QS system ComQXPA activates the transcription of hundreds of genes, including the srfA operon and competence genes (Weinrauch et al, 1990; Roggiani and Dubnau, 1993; Magnuson et al, 1994). ComS stops proteolytic degradation of ComK (Turgay et al, 1998) that increases in concentration and activates the transcription of late competence genes that encode processes responsible for the DNA uptake and integration (Dubnau, 1991). This state has been referred to as the K-state (Berka et al, 2002). Undomesticated strain cotA:cat skfA:spec srfA:Tn917 (mls) srfA:Tn917 (mls) cotA:cat srfA:Tn917 (mls) skfA:spec amyE:P43-lacZ (Kn) srfA:Tn917 (mls) amyE:P43-lacZ (Kn) amyE:Phyperspank -mKate (Cm) trpC2 cotA:cat skfA:spec pheA1 sfp srfA:Tn917 (mls) amyE:P43-yfp (Spec, Amp) pBKT2 amyE:lacZ (Kn, Amp) pBKT2 amyE:P43-lacZ (Kn, Amp)

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