Microbial community structure and dynamics on patchy landscapes

Thesis: Ph. D., Massachusetts Institute of Technology, Computational and Systems Biology Program, 2016.This electronic version was submitted by the student author. The certified thesis is available in the Institute Archives and Special Collections.Cataloged from student-submitted PDF version of thesis.Includes bibliographical references (pages 139-156).Microbes are tiny metabolic engines with large-scale effects on industry, the environment, and human health. Understanding how the micron-scale actions (and interactions) of individual microbes give rise to macro-scale consequences remains a major challenge in microbial ecology. However, for the most part, studies employ coarsegrained sampling schemes, which average over the heterogeneous microscopic structure of microbial communities. This has limited our ability to establish mechanistic links between dynamics occurring across these disparate spatial scales. However, such links are critical for (a) making sense of the tremendous extant microbial diversity on Earth, and (b) predicting how perturbations (e.g., global climate change) may influence microbial diversity and function. In this thesis, I characterize the structure and dynamics of wild bacterial populations in the ocean at spatial scales of tens of microns. I then employ a simple, two-strain laboratory model system to link (cooperative) inter-species interactions at local scales to emergent properties at larger scales, focusing on spatially connected meta-communities undergoing range expansions into new territory. This work encompasses diverse environments (ranging from well-mixed communities in the laboratory to individual crustaceans) and approaches (including mathematical modeling, highthroughput sequencing, and traditional microbiological experiments). Altogether, we find that the microscale environment inhabited by a microbe - that is, "what the neighborhood is like" and "who lives next to whom" - shapes the structure and dynamics of wild microbial populations at local scales. Moreover, these local interactions can drive patterns of biodiversity and function, even at spatial scales much larger than the length of an individual cell. Thus, our work represents a small step toward developing mechanistic theories for how microbes shape our planet's ecosystems.by Manoshi Sen Datta.Ph. D

Microbial interactions and community assembly at microscales

In most environments, microbial interactions take place within microscale cell aggregates. At the scale of these aggregates (∼100 μm), interactions are likely to be the dominant driver of population structure and dynamics. In particular, organisms that exploit interspecific interactions to increase ecological performance often co-aggregate. Conversely, organisms that antagonize each other will tend to spatially segregate, creating distinct micro-communities and increased diversity at larger length scales. We argue that, in order to understand the role that biological interactions play in microbial community function, it is necessary to study microscale spatial organization with enough throughput to measure statistical associations between taxa and possible alternative community states. We conclude by proposing strategies to tackle this challenge

Microbial interactions lead to rapid micro-scale successions on model marine particles

In the ocean, organic particles harbour diverse bacterial communities, which collectively digest and recycle essential nutrients. Traits like motility and exo-enzyme production allow individual taxa to colonize and exploit particle resources, but it remains unclear how community dynamics emerge from these individual traits. Here we track the taxon and trait dynamics of bacteria attached to model marine particles and demonstrate that particle-attached communities undergo rapid, reproducible successions driven by ecological interactions. Motile, particle-degrading taxa are selected for during early successional stages. However, this selective pressure is later relaxed when secondary consumers invade, which are unable to use the particle resource but, instead, rely on carbon from primary degraders. This creates a trophic chain that shifts community metabolism away from the particle substrate. These results suggest that primary successions may shape particle-attached bacterial communities in the ocean and that rapid community-wide metabolic shifts could limit rates of marine particle degradation.American Society for Engineering Education. National Defense Science and Engineering Graduate FellowshipNational Science Foundation (U.S.) (CAREER Award PHY-1055154)European Research Council (Starting Grant 336938)National Science Foundation (U.S.). Division of Ocean Sciences (Award 14359930

Modular Assembly of Polysaccharide-Degrading Marine Microbial Communities

Understanding the principles that govern the assembly of microbial communities across earth's biomes is a major challenge in modern microbial ecology. This pursuit is complicated by the difficulties of mapping functional roles and interactions onto communities with immense taxonomic diversity and of identifying the scale at which microbes interact [1]. To address this challenge, here, we focused on the bacterial communities that colonize and degrade particulate organic matter in the ocean [2–4]. We show that the assembly of these communities can be simplified as a linear combination of functional modules. Using synthetic polysaccharide particles immersed in natural bacterioplankton assemblages [1, 5], we showed that successional particle colonization dynamics are driven by the interaction of two types of modules: a first type made of narrowly specialized primary degraders, whose dynamics are controlled by particle polysaccharide composition, and a second type containing substrate-independent taxa whose dynamics are controlled by interspecific interactions—in particular, cross-feeding via organic acids, amino acids, and other metabolic byproducts. We show that, as a consequence of this trophic structure, communities can assemble modularly—i.e., by a simple sum of substrate-specific primary degrader modules, one for each complex polysaccharide in the particle, connected to a single broad-niche range consumer module. Consistent with this model, a linear combination of the communities on single-polysaccharide particles accurately predicts community composition on mixed-polysaccharide particles. Our results suggest that the assembly of heterotrophic communities that degrade complex organic materials follows simple design principles that could be exploited to engineer heterotrophic microbiomes. Enke et al. show that particle-attached marine microbial communities assemble by recruiting functional groups of taxa in an additive manner. Specialist groups degrade specific polysaccharides, whereas generalist byproduct utilizers invade independently of particle substrate. This simple organization allows prediction of community structure.Simons Foundation. Simons Early Career Award (410104)Alfred P. Sloan Foundation. Fellowship (FG-20166236)National Science Foundation (U.S.) (Grant OCE-1658451)Simons Collaboration: Principles of Microbial Ecosystems (PriME) (Award 542395

Adaptive radiation by waves of gene transfer leads to fine-scale resource partitioning in marine microbes

Adaptive radiations are important drivers of niche filling, since they rapidly adapt a single clade of organisms to ecological opportunities. Although thought to be common for animals and plants, adaptive radiations have remained difficult to document for microbes in the wild. Here we describe a recent adaptive radiation leading to fine-scale ecophysiological differentiation in the degradation of an algal glycan in a clade of closely related marine bacteria. Horizontal gene transfer is the primary driver in the diversification of the pathway leading to several ecophysiologically differentiated Vibrionaceae populations adapted to different physical forms of alginate. Pathway architecture is predictive of function and ecology, underscoring that horizontal gene transfer without extensive regulatory changes can rapidly assemble fully functional pathways in microbes.United States. Department of Energy (DE-SC0008743)National Defense Science and Engineering Graduate (NDSEG) Fellowshi