Bacterial-induced pH shifts link individual cell physiology to macroscale collective behavior

Abstract

Bacteria have evolved a diverse array of signaling pathways that enable them to quickly respond to environmental changes. Understanding how these pathways reflect environmental conditions and produce an orchestrated response is an ongoing challenge. Herein, we present a role for collective modifications of environmental pH carried out by microbial colonies living on a surface. We show that by collectively adjusting the local pH value, Paenibacillus spp., specifically, regulate their swarming motility. Moreover, we show that such pH-dependent regulation can converge with the carbon repression pathway to down-regulate flagellin expression and inhibit swarming in the presence of glucose. Interestingly, our results demonstrate that the observed glucose-dependent swarming repression is not mediated by the glucose molecule per se, as commonly thought to occur in carbon repression pathways, but rather is governed by a decrease in pH due to glucose metabolism. In fact, modification of the environmental pH by neighboring bacterial species could override this glucose-dependent repression and induce swarming of Paenibacillus spp. away from a glucose-rich area. Our results suggest that bacteria can use local pH modulations to reflect nutrient availability and link individual bacterial physiology to macroscale collective behavior.

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“…Similarly, plants could act as mediators and connect microbial metapopulations via VOCs, potentially leading to VOC-mediated interdependences and metarhizobiome stability at the landscape level, highlighting the importance of Gamma diversity. For example, Dharanishanthi et al ( 69 ) reported that modification of the environmental pH by neighboring bacterial species could be used as a clue about nutrient availability by local bacteria, linking individual bacterial physiology to macroscale collective behavior.…”

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“…S13 ). This phenomenon has been observed in other bacteria that secrete organic acids from glucose metabolism, such as lactic, acetic, succinic, and pyruvic acid, causing rapid extinction of the entire population due to the lowered pH of the environment [ 14 , 15 , 56 , 77 – 79 ]. In contrast, DT-2, with a defective hexokinase and phosphotransferase system, efficiently utilizes pyruvic acid as a carbon source (Fig.…”

“…S22). These observations suggest that many Bacillus species may have the ability to generate pyruvic acid from glucose, thereby acidifing their growth environment [15,[56][57][58][59]. These bacteria also arsM gene in their genomes, which enables the methylation of MAs(III).…”

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