Stressed-Out Soil Bacteria Adapt to Environmental Conditions

A new study from Caltech demonstrates that soil bacteria can adapt under stress, particularly when a key nutrient, phosphorus, is running low in their environment. The work is important for understanding the complex relationships between microorganisms and the roots of plants, which has implications for soil health and food sustainability as the climate changes.

The work was conducted in the laboratory of Dianne Newman, the Gordon M. Binder/Amgen Professor of Biology and Geobiology, and is described in a new paper appearing in the journal Current Biology on June 19.

Quorum sensing is a molecular signaling system that acts as way for bacteria to communicate and coordinate their behavior. Bacteria are constantly secreting signaling molecules into their surroundings, and when these molecules accumulate to a certain concentration, typically associated with a high cell density, quorum-sensing responses can be triggered. In this way, bacteria know what is happening around them and when to initiate certain behaviors. For example, a high density of neighboring cells might mean that nearby nutrients are getting gobbled up, prompting bacteria to produce compounds that help them better survive stress or compete for nutrients.

One such class of helpful compounds are phenazines, which are produced when particular quorum-sensing thresholds are reached. Phenazines have several different functions, like a Swiss Army knife: They can help a cell acquire nutrients, compete with neighbors, and serve other roles to support the cell's survival. Which role they play depends on the circumstances.

In the new study, the team examined how the soil-associated bacterium Pseudomonas synxantha produces phenazines in lab environments that model soil conditions, particularly when the bacteria lack phosphorus, a key nutrient that is often difficult to come by in soils. Even when phosphorus is present, it is often tied up in forms that bacteria and plants cannot easily use. This makes phosphorus scarcity an ecologically relevant condition under which to study how soil microbes adjust their behavior.

"Recently, we have gotten interested in understanding how phenazines affect microbial communities in soils—the natural habitat for phenazine-producing bacteria," Newman says. "Previously, we had observed that phenazine production is stimulated when bioavailable phosphorus is scarce, but we didn't understand how this worked through mechanisms of quorum sensing."

When phosphorus is in low supply in the bacteria's environment, the team found that quorum sensing is triggered at much lower population densities and signaling molecule concentrations. Because of this, bacteria can produce phenazines even if their environment is not as crowded.

"Much of our mechanistic understanding of bacterial communication comes from simplified laboratory systems," says postdoctoral scholar Reinaldo Alcalde, the study's first author. "But soils are physically and chemically complex. By adding that context back in, we can better understand how bacteria behave where they actually live."

The research is particularly relevant for understanding natural soil systems, where bacteria tend to have more sparse populations than in lab settings. Testing environmentally relevant conditions (like phosphorus scarcity) gives a better picture of what is happening, for example, around plant roots where nutrients and water are unevenly distributed.

Quorum sensing is a behavior shared by many bacteria, not just Pseudomonas.

"Our work shows that the environment tunes quorum-sensing thresholds," Alcalde says. "When a key nutrient is scarce, bacteria can become more responsive to chemical signals and change the rules for when they invest in collective behaviors."

Newman's laboratory has a decades-long history of studying phenazines and a broad interest in understanding the behavior of microbes in the soil. In 2024, Alcalde collaborated with biophotonics specialist Oumeng Zhang, at the time a postdoctoral scholar in the laboratory of Changhuei Yang (Caltech's Thomas G. Myers Professor of Electrical Engineering, Bioengineering, and Medical Engineering; Heritage Medical Research Institute Investigator; and executive officer for electrical engineering), to design and build a microscope from scratch, using funds provided by Caltech's Center for Environmental Microbial Interactions, the Ronald and Maxine Linde Center for Global Environmental Science, and the Resnick Sustainability Institute at Caltech. Zhang and Alcalde designed a light-sheet fluorescence microscope specifically tailored to generate live 3D images of root systems to watch the interactions between roots and microbes in real time in a naturally opaque environment.

"Rei came to Caltech with a PhD in environmental engineering, and over the course of these projects, maximized his research opportunities," Newman says. "Not only did he learn how to manipulate bacteria genetically in my lab, but he also learned about optical engineering through his collaboration with Oumeng. They did things together that neither would have done alone. Their friendship and creative partnership exemplify the good things that Caltech can catalyze."

Though Alcalde and Zhang are both moving on to different institutions after their postdoctoral appointments, they plan to continue their collaboration. Meanwhile, researchers in the Newman lab plan to further examine the relationship between microbes and their metabolites in root systems.

The paper is titled "Phosphorus stress and spatial confinement lower the quorum-sensing activation threshold for phenazine production in Pseudomonas synxantha." In addition to Alcalde, Zhang, Newman, and Yang, Caltech co-authors are postdoctoral scholar Hannah Jeckel; graduate student Rogelio Avila; and Nathan Dalleska, lead laboratory administrator of the Linde Center. Dmitri Mavrodi of the US Department of Agriculture is also a co-author. Funding was provided by the Resnick Sustainability Institute, the Caltech Beckman Institute, the Arnold and Mabel Beckman Foundation, the National Science Foundation, and a Helen Hay Whitney Foundation postdoctoral fellowship.