Enhanced niche colonisation and competition during bacterial adaptation to a fungus

Author:

Richter Anne,Blei Felix,Hu GuohaiORCID,Schwitalla Jan W.ORCID,Lozano-Andrade Carlos N.ORCID,Jarmusch Scott AORCID,Wibowo MarioORCID,Kjeldgaard BodilORCID,Surabhi SurabhiORCID,Jautzus TheresaORCID,Phippen Christopher B. W.ORCID,Tyc OlafORCID,Arentshorst MarkORCID,Wang YueORCID,Garbeva PaolinaORCID,Larsen Thomas OstenfeldORCID,Ram Arthur F.J.ORCID,van den Hondel Cees A.M.ORCID,Maróti GergelyORCID,Kovács Ákos T.ORCID

Abstract

AbstractBacterial-fungal interactions (BFIs) influence microbial community performance of most ecosystems and elicit specific microbial behaviours, including stimulating specialised metabolite production. Using a simple BFI system encompassing the Gram-positive bacteriumBacillus subtilisand the black mould fungusAspergillus niger, we established a co-culture experimental evolution method to investigate bacterial adaptation to the presence of a fungus. In the evolving populations,B. subtiliswas rapidly selected for enhanced production of the lipopeptide surfactin and accelerated surface spreading ability, leading to inhibition of fungal expansion and acidification of the environment. These phenotypes were explained by specific mutations in the DegS-DegU two-component system. In the presence of surfactin, fungal hyphae exhibited bulging cells with delocalised secretory vesicles and RlmA-dependent cell wall stress induction. Increased surfactin production typically enhances the competitive success of bacteria against fungi, which likely explains the primary adaption path in the presence ofA. niger.Significance statementExperimental evolution and co-cultivation of different microbes are important and useful techniques for discovering new traits and unravelling cryptic regulatory connections. We combined these methods by evolving the Gram-positive bacteriumBacillus subtilisin the presence of the black mould fungusAspergillus nigerthat were previously shown to engage in an intricate and physical interaction. Both are ubiquitous, environmentally and industrially relevant model microbes in the colonisation of rhizo- and endosphere and in the production of enzymes. Our results demonstrate how laboratory adaptation can be exploited to improve biocontrol properties of bacteria.

Publisher

Cold Spring Harbor Laboratory

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