Abstract
Many microbes exhibit quorum sensing (QS) to cooperate, share and perform a social task in unison. Recent studies have shown the emergence of reversible phenotypic heterogeneity in the QS-responding pathogenic microbial population under laboratory conditions as a possible bet-hedging survival strategy. However, very little is known about the dynamics of QS-response and the nature of phenotypic heterogeneity in an actual host-pathogen interaction environment. Here, we investigated the dynamics of QS-response of a Gram-negative phytopathogen Xanthomonas pv. campestris (Xcc) inside its natural host cabbage, that communicate through a fatty acid signal molecule called DSF (diffusible signal factor) for coordination of several social traits including virulence functions. In this study, we engineered a novel DSF responsive whole-cell QS dual-bioreporter to measure the DSF mediated QS-response in Xcc at the single cell level inside its natural host plant in vivo. Employing the dual-bioreporter strain of Xcc, we show that QS non-responsive cells coexist with responsive cells in microcolonies at the early stage of the disease; whereas in the late stages, the QS-response is more homogeneous as the QS non-responders exhibit reduced fitness and are out competed by the wild-type. Furthermore, using the wild-type Xcc and its QS mutants in single and mixed infection studies, we show that QS mutants get benefit to some extend at the early stage of disease and contribute to localized colonization. However, the QS-responding cells contribute to spread along xylem vessel. These results contrast with the earlier studies describing that expected cross-induction and cooperative sharing at high cell density in vivo may lead to synchronize QS-response. Our findings suggest that the transition from heterogeneity to homogeneity in QS-response within a bacterial population contributes to its overall virulence efficiency to cause disease in the host plant under natural environment.
Highlights
Pathogenic bacteria coordinate several social behaviors via production, secretion and perception of diverse diffusible cell-cell signaling molecules by a process called quorum sensing (QS)
QSresponse and regulation has been studied under laboratory conditions in vitro, where the QS mutants (QS-)responding bacterial population exhibits heterogeneous QS-response with the emergence of both QS responders and non-responders irrespective of their parental kind, as a possible bet hedging strategy
Using Xanthomonas campestris pv. campestris (Xcc) and cabbage as a model plant pathogen-host, we show that there is stage specific interplay of heterogeneous and homogeneous QS-response in the wild-type Xcc population inside the host plant
Summary
Pathogenic bacteria coordinate several social behaviors via production, secretion and perception of diverse diffusible cell-cell signaling molecules by a process called quorum sensing (QS). QS synchronizes the bacteria to perform social task in unison by coordinating production of exo-products as ‘public goods’ that are beneficial to the population as a whole. Such social tasks include the production of virulence associated function-components involved in biofilm formation, extracellular enzymes, extracellular polysaccharide and surfactants that promote motility and spread [1, 2, 3, 4]. QS has been associated with cooperation at high cell density, recent experimental and theoretical modelling studies in pathogenic bacteria such as Pseudomonas, Vibrio and Xanthomonas have demonstrated that QS-response is complex; as bacteria exhibit reversible non-genetic phenotypic heterogeneity in QS-response generating two distinct sub-populations of QS-responsive and non-responsive cells under artificial laboratory conditions [8, 9, 10, 11]. Heterogeneity in performing social task may have adaptive functions, such as division of labour and sharing of environmental resources
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