Regulatory Rewiring Drives Intraspecies Competition in Bacillus subtilis

TY - JOUR

T1 - Regulatory Rewiring Drives Intraspecies Competition in Bacillus subtilis

AU - Kalamara, Margarita

AU - Bonsall, Alistair

AU - Griffin, Jonathan

AU - Carneiro, Joana

AU - Gierlinski, Marek

AU - Eigentler, Lukas

AU - Stevenson, David

AU - Wood, Amy

AU - Porter, Michael

AU - Dorfmueller, Helge

AU - MacPhee, Cait E.

AU - Abbott, James

AU - Stanley-Wall, Nicola

N1 - Publisher Copyright: Copyright: © 2026 Kalamara et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

PY - 2026/2/17

Y1 - 2026/2/17

N2 - Intraspecies interactions shape microbial community structure and evolution, yet the mechanisms determining competitive outcomes among closely related strains remain unclear. The soil bacterium Bacillus subtilis is a model for microbial social interactions, where quorum-sensing systems regulate cooperation and antagonism. Here, we take a multifaceted approach to dissect the role of quorum-sensing regulation in competitive fitness. Isolate NCIB 3610 carries a signal unresponsive RapP-PhrP module that alters quorum-sensing control and promotes faster growth. Modelling and mutant analysis demonstrate that the small differences in growth rate conferred by RapP-PhrP3610 are sufficient to drive competitive exclusion. The importance of quorum sensing control is further exemplified by experimental evolution of distinct wild isolates, which revealed recurrent mutations in the sensor kinase comP, which phenocopy complete comP or comA deletions and confer a growth-linked competitive advantage. Key quorum sensing mechanisms are abandoned even in structured microbial communities, where it might be expected that communal traits are favoured. Furthermore, a phylogenomic survey of 370 B. subtilis genomes identified disruptive comP mutations in ~16% of isolates. However, growth rate alone does not explain all interaction outcomes as even isogenic strains with equivalent doubling times differ in competitiveness. Transcriptomic profiling and validation experiments implicated a type VII secretion system toxin as an additional effector. These findings reveal that disruption of quorum-sensing pathways, whether naturally or through selection, provides a rapid route to competitive advantage, highlighting a fundamental trade-off between communal signalling and individual fitness in microbial populations.

AB - Intraspecies interactions shape microbial community structure and evolution, yet the mechanisms determining competitive outcomes among closely related strains remain unclear. The soil bacterium Bacillus subtilis is a model for microbial social interactions, where quorum-sensing systems regulate cooperation and antagonism. Here, we take a multifaceted approach to dissect the role of quorum-sensing regulation in competitive fitness. Isolate NCIB 3610 carries a signal unresponsive RapP-PhrP module that alters quorum-sensing control and promotes faster growth. Modelling and mutant analysis demonstrate that the small differences in growth rate conferred by RapP-PhrP3610 are sufficient to drive competitive exclusion. The importance of quorum sensing control is further exemplified by experimental evolution of distinct wild isolates, which revealed recurrent mutations in the sensor kinase comP, which phenocopy complete comP or comA deletions and confer a growth-linked competitive advantage. Key quorum sensing mechanisms are abandoned even in structured microbial communities, where it might be expected that communal traits are favoured. Furthermore, a phylogenomic survey of 370 B. subtilis genomes identified disruptive comP mutations in ~16% of isolates. However, growth rate alone does not explain all interaction outcomes as even isogenic strains with equivalent doubling times differ in competitiveness. Transcriptomic profiling and validation experiments implicated a type VII secretion system toxin as an additional effector. These findings reveal that disruption of quorum-sensing pathways, whether naturally or through selection, provides a rapid route to competitive advantage, highlighting a fundamental trade-off between communal signalling and individual fitness in microbial populations.

KW - Bacillus subtilis

KW - Intraspecies competition

KW - Quorum sensing

KW - ComQXPA system

KW - Experimental evolution

KW - Regulatory rewiring

KW - Sensor kinase mutations

UR - https://www.scopus.com/pages/publications/105031381937

U2 - 10.1371/journal.pgen.1012050

DO - 10.1371/journal.pgen.1012050

M3 - Article

C2 - 41701782

SN - 1553-7390

VL - 22

SP - e1012050

JO - PLoS Genetics

JF - PLoS Genetics

IS - 2

M1 - e1012050

ER -