Revealing the Hidden Powers of Microbial pH Sensing: A Revolutionary Discovery in Environmental Adaptation

Researchers at Vanderbilt University have found that laboratory evolved pH-sensitive mutations in bacteria rapidly confer transcriptional responses to the environment’s shift in pH, mimicking patterns seen for natural pathogens and marine organisms. 

A study led by Sarah Worthan, PhD, Vanderbilt University’s Behringer Lab, explores the ways in which microbial cultures selectively evolve to detect pH fluctuations: a rapid adaptation to the permutations of their environment. The study, which appears in the online early edition of the Proceedings of the National Academy of Sciences on September 19, 2024, shines a spotlight on lab-evolved traits that mirror mutations in nature, such as those in emerging pathogens and coral symbionts in extreme pH shifts in the surroundings.

Lab-Driven Evolution Leads to the Emergence of pH-Sensitive Mutations

The team isolated a mutation that operated continually in bacteria under intense starvation cycles. The mutation included the substitution of an arginine (Arg) amino acid with a histidine (His); this mutated form directly impacts the RNA-binding capability of the Rho protein, a transcription termination factor. This mutation, unlike traditional forms of cell signaling, causes a fast transcriptional response to pH shifts from more alkaline to neutral environments.

Co-author Benjamin Bratton, Ph.D., of the Vanderbilt University Medical Center led imaging analysis, while Centre de Biophysique Moléculaire in France’s Marc Boudvillain, Ph.D., showed how the Arg-to-His mutation allows the activity of Rho protein to be controlled in a pH-dependent manner. Such pH dependent bypassing of conventional signaling and direct response to changes in environmental pH underscores one evolutionary adaptation of considerable importance. Such mutations may represent an integral component of coordinating fast cellular responses under fluctuating conditions, a challenge both microorganisms and larger organisms alike have to live with.

Discovery Reaches the Natural Systems

Building on their laboratory findings, the researchers discovered comparable pH-sensing mutations in nature. They found this mutation in Bartonella baciliformis, a pathogen causing Carrion’s Disease in South America. That bacterium must quickly change its pH sensing as it transitions from the insect gut’s high pH to human blood’s neutral pH. The same ability, which represents the sense and response to pH changes, was also detected in marine environments where microorganisms, including those in hydrothermal vents and in sponge bodies, have to adjust to pH levels that fluctuate widely.

Implications of pH-Sensitive Mutations in a Changing Climate

These findings have wide-ranging implications far beyond the lab. For example, if climatic conditions change ocean pH, it could throw off the adaptive microbial systems and “could throw off the delicate balance of microbial symbiosis,” Worthan said, referring to how, in that event, if the pH of the ocean began to resemble that of sponges

This is the validation of lab-driven evolution and offers crucial insights into the ways that microorganisms adapt to environmental pressures. Mutations in the global regulators, thus, making them sensitive to the pH of their surroundings, can be a novel discovery – possibly in RNA- or DNA-binding proteins. As they could be engineered to respond almost immediately to returning environmental challenges, possibilities would then open in environmental monitoring, bioprocessing, or medical applications. Such collaboration between molecular biologists, biochemists, and evolutionary response-studying scientists opens avenues towards facing life’s complexities dynamically in dynamic ecosystems.

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