Ocean Acidification: Impacts of Evolution on the Response of Phytoplankton Populations to Rising CO2

Human activities are driving up atmospheric carbon dioxide concentrations at an unprecedented rate, perturbing the ocean's carbonate buffering system, lowering oceanic pH, and changing the concentration and composition of dissolved inorganic carbon. Recent studies have shown that this ocean acidification has many short-term effects on phytoplankton, including changes in carbon fixation among others. These physiological changes could have profound effects on phytoplankton metabolism and community structure, with concomitant effects on Earth's carbon cycle and, hence, global climate. However, extrapolation of present understanding to the field are complicated by the possibility that natural populations might evolve in response to their changing environments, leading to different outcomes than those predicted from short-term studies. Indeed, evolution experiments demonstrate that microbes are often able to rapidly adapt to changes in the environment, and that beneficial mutations are capable of sweeping large populations on time scales relevant to predictions of environmental dynamics in the coming decades. This project addresses two major areas of uncertainty for phytoplankton populations with the following questions: 1) What adaptive mutations to elevated CO2 are easily accessible to extant species, how often do they arise, and how large are their effects on fitness? 2) How will physical and ecological interactions affect the expansion of those mutations into standing populations? This study will address these questions by coupling experimental evolution with computational modeling of ocean biogeochemical cycles. First, cultured unicellular phytoplankton, representative of major functional groups (e.g. cyanobacteria, diatoms, coccolithophores), will be evolved under simulated year 2100 CO2 concentrations. From these experiments, estimates will be made of a) the rate of beneficial mutations, b) the magnitude of fitness gains conferred by these mutations, and c) secondary phenotypes (i.e., trade-offs) associated with these mutations, assayed using both physiological and genetic approaches. Second, an existing numerical model of the global ocean system will be modified to a) simulate the effects of changing atmospheric CO2 concentrations on ocean chemistry, and b) allow the introduction of CO2-specific adaptive mutants into the extant populations of virtual phytoplankton. The model will be used to explore the ecological and biogeochemical impacts of beneficial mutations in realistic environmental situations (e.g. resource availability, predation, etc.). Initially, the model will be applied to idealized sensitivity studies; then, as experimental results become available, the implications of the specific beneficial mutations observed in our experiments will be explored.

Broader Impacts: This interdisciplinary study will provide novel, transformative understanding of the extent to which evolutionary processes influence phytoplankton diversity, physiological ecology, and carbon cycling in the near-future ocean. One of many important outcomes will be the development and testing of nearly-neutral genetic markers useful for competition studies in major phytoplankton functional groups, which has applications well beyond the current proposal. An inherent component of the proposed work is the integration of education and outreach to provide advanced interdisciplinary training to undergraduate students, while involving both them and the PIs in community outreach and education related to ocean acidification. At MSU, undergraduate students will participate in bench work as well as computer modeling, and will therefore gain interdisciplinary research experience. Among other projects, these students will produce a simplified version of the ocean modeling software that may be implemented as an "app" for use with education and outreach programs. At least two additional undergraduates will be recruited to work on the project at Columbia and MIT, with a focus on broadening participation in STEM through hands-on training. Additionally, visits with secondary education institutes will be arranged to talk about ocean acidification and microbial "evolution in action." These visits will be facilitated by instructional resources focused on ocean acidification, microbiology, and evolution, which are available from two NSF STCs, BEACON (MSU) and CMORE (MIT/Columbia).