Project: Characterizing the effects of exogenous reactive oxygen species on marine microbial ecosystem dynamics

NSF Award Abstract:
The microbes that constitute the phytoplankton community of the ocean account for about half of all photosynthesis on the earth and as a consequence are critically important to the climate and major nutrient cycles of the planet. The vast majority of the ocean surface is relatively depleted in nutrients essential for organisms to grow. This is especially true for the ocean gyres that are hundreds or thousands of miles from the coast and thousands of meters above the ocean floor. In these regions, competition among different phytoplankton for nutrients is thought to be especially strong. The most abundant member of the photosynthetic community, the single-celled bacterium Prochlorococcus, is also its smallest, measuring a half a micrometer in length. Interestingly, Prochlorococcus is very sensitive to reactive oxygen species (ROS) such as hydrogen peroxide and cannot grow in the absence of “helper” microbes which detoxify the ROS generated when sunlight reacts with pigmented organic material in the seawater. The true extent to which Prochlorococcus depends on helpers is currently unknown: thus far, experiments have only assessed Prochlorococcus survival of ROS stress under otherwise optimal growth conditions which are rare in the natural environment. Recent evidence that Prochlorococcus and helpers can compete for nutrients adds another layer of complexity. This project combines experimental culture work, field measurements, and ecosystem modeling to characterize the roles of ROS in surface ocean community dynamics. Laboratory cultures of Prochlorococcus and other microbes are being examined for growth and survival changes when exposed to ROS under a range of nutrient concentrations, temperatures, and light intensities, when grown separately and in co-culture with each other. Outcomes from the laboratory experiments are then being used in mathematical ecosystem models to simulate the natural marine environment. Finally, laboratory results and mathematical models are being compared to natural communities in the North Pacific Ocean exposed to a range of ROS concentrations. In this way, this research is developing a deeper and more predictive understanding of how microbial community composition and mortality depend upon ROS production and decay. Broader impacts of the project include the training of undergraduate and graduate students in oceanographic research and public outreach about microbiology and oceanography to the local Knoxville community, as well as dependents of active duty Marines.

The overarching goal of this project is to empirically parameterize ecosystem models using a combination of lab experiments and field manipulations to explore the coupled dynamics of HOOH and oligotrophic microbial communities. Prochlorococcus is the most abundant phytoplankter in the oligotrophic ocean and contributes significantly to global carbon cycling. Key to its abundance is its ability to outcompete other microbes for nutrients. This ecological advantage is thought to involve an evolutionary process of genomic streamlining, including a loss of hydrogen peroxide (HOOH) resistance mechanisms and reliance of Prochlorococcus on the microbial community to degrade photochemically-generated HOOH in the sun-exposed surface mixed layer. When temperature deviates from optimal, however, sensitivity of Prochlorococcus to HOOH – and thus reliance upon helpers - is heightened. The same may hold true for light and nutrient conditions. Similarly, little is known about the environmental sensitivity of HOOH-detoxifying “helper” microbes, including fellow members of the phytoplankton community. Therefore, the extent to which Prochlorococcus requires help, and to which different HOOH-consuming microbes provide this function, is not currently understood. This project is providing the quantitative measurements in HOOH and microbial dynamics to understand the rules of microbial community assembly in the surface mixed layer. Several strains of Prochlorococcus, potential helper, and competitor microbes are being grown under a range of nutrient-limiting and HOOH conditions in chemostats to assess growth, mortality, and - for the phytoplankton – photosynthesis. Co-cultures with the other microbes, including Synechococcus and several photosynthetic picoeukaryotes, are being used to test hypotheses about HOOH detoxification and the impacts of competition on Prochlorococcus–ROS dynamics under optimal and suboptimal conditions These ecosystem model predictions are being interpreted alongside field manipulations which directly assess ROS mediated impacts in the context of other loss processes, primarily grazing and viral lysis.

This award reflects NSF's statutory mission and has been deemed worthy of support through evaluation using the Foundation's intellectual merit and broader impacts review criteria.