Award: OCE-1658451

Marine bacteria play key roles in the cycling of nutrients on Earth. Many of these microorganisms carry delicate adaptations that allow them to biodegrade complex forms of organic matter found on marine particles. Degradating these particles is essential to maintaining life of earth, because otherwise organic matter would sink to the bottom of the ocean floor, sequestering carbon and nitrogen essential for life on the planet. One of the most fascinating aspects of this process is that, in order to degrade particles, bacteria assemble onto diverse ecological communities on particle surfaces, where interactions between species can have large impacts on degradation rates. This interplay between community assembly and ecosystem function was the main area of research addressed in this project. Our work showed that the dynamics of community assembly on marine particles follow successions (Datta 2016, Enke 2019), similar to those described many decades ago for forest and other plant ecosystems. This is a remarkable comparison, because while forests span tens or hundreds of kilometers, a particle has a diameter of tens of microns. Successions imply that the community assembles in stages, where some species dominate at early timepoints, followed by a different set of species, and so on until the system reaches a climax. In the case of marine particles, the successions start with those bacteria that can degrade the particle substrate, but rapidly turn into communities dominated by bacteria that grow from the metabolic waste products of those early colonizers. Therefore, the ecological process by which a community assembles on particles is driven by microbial interactions that shift the state of the community from one being dominated by degraders, to one being dominated by secondary consumers that cannot break down the complex polymers stored on particles. The consequence of this transition in community composition is a slowdown of the particle degradation process. We showed this using a laboratory model system based on new techniques developed in my lab in the context of this project (Enke 2018). In particular, using time-lapse imaging of synthetic particles we were able to quantify changes in particle volume resulting from the activity of microbes. This data also allowed us to build mathematical models that describe the dynamics of particle degradation and bacterial growth. In summary, one of the main contributions of our work was to establish that microbial interactions on particles can actually have a significant impact on a key ecosystem process, in this case the turnover of organic matter in the ocean. The work I have described so far was based on chitin, a particular biopolymer of great relevance in oceans and soils. However, we wanted to understand how the process would change with other relevant substrates, or even more interesting, with combinations of relevant biopolymers, since in nature organic matter is composed of a combination of these materials. To this end, we manufactured synthetic marine particles made of combinations of algal polysaccharides. We found that we were able to predict community composition using simple mathematical models (Enke and Datta, 2019). Based on these results, we proposed that communities assemble in a modular fashion: by recruiting groups of species specialized in degrading specific polysaccharides. For each polysaccharide there was a group of specialists. In addition, there was a group of generalist secondary consumers growing on metabolic byproducts. The ability to synthetize the community in these simple terms is a major advance over the current practice of simply enumerating lists of species. Overall, our research project has laid a foundation to better understand how microbial interactions impact key ecosystem processes, namely the cycling of carbon in the planet. Our main contributions were the development of model systems that allowed us to measure community assembly in a precise manner and to quantify the impact of microbial interactions on particle degradation kinetics. This is a significant departure from current practice, which is centered primarily on field observations, an approach that makes it extremely hard to obtain quantitative data of community assembly or degradation kinetics. Furthermore, our work has led to the development of important resources, such as a collection of marine isolates that specialize in particle degradation. This resource is currently being applied to understand the physiology of particle-associated marine bacteria. Last Modified: 01/14/2021 Submitted by: Otto X Cordero Sanchez