Microbial communities are inherently complex systems. To address this complexity, microbial ecologists are developing new, more elaborate laboratory models at an ever-increasing pace.
Abstract Sinking marine particles drive the biological pump that naturally sequesters carbon from the atmosphere. Despite their small size, the compartmentalized nature of particles promotes intense localized metabolic activity by their bacterial colonizers. Yet the mechanisms promoting the onset of denitrification, a metabolism that arises once oxygen is limiting, remain to be established. Here we show experimentally that slow sinking aggregates composed of marine diatoms—important primary producers for global carbon export—support active denitrification even among bulk oxygenated water typically thought to exclude anaerobic metabolisms. Denitrification occurs at anoxic microsites distributed throughout a particle and within microns of a particle’s boundary, and fluorescence-reporting bacteria show nitrite can be released into the water column due to segregated dissimilatory reduction of nitrate and nitrite. Examining intact and broken diatoms as organic sources, we show slowly leaking cells promote more bacterial growth, allow particles to have lower oxygen, and generally support greater denitrification.
Surface-attached microbial communities consist of different cell types that, at least to some degree, organize themselves non-randomly across space (referred to as spatial self-organization). While spatial self-organization can have important effects on the functioning, ecology and evolution of communities, the underlying determinants of spatial self-organization remain unclear. Here, we hypothesize that the presence of physical objects across a surface can have important effects on spatial self-organization. Using pairs of isogenic strains of Pseudomonas stutzeri , we performed range expansion experiments in the absence or presence of physical objects and quantified the effects on spatial self-organization. We demonstrate that physical objects create local deformities along the expansion frontier, and these deformities increase in magnitude during range expansion. The deformities affect the densities of interspecific boundaries and diversity along the expansion frontier, and thus affect spatial self-organization, but the effects are interaction-dependent. For competitive interactions that promote sectorized patterns of spatial self-organization, physical objects increase the density of interspecific boundaries and diversity. By contrast, for cross-feeding interactions that promote dendritic patterns, they decrease the density of interspecific boundaries and diversity. These qualitatively different outcomes are probably caused by fundamental differences in the orientations of the interspecific boundaries. Thus, in order to predict the effects of physical objects on spatial self-organization, information is needed regarding the interactions present within a community and the general geometric shapes of spatial self-organization that emerge from those interactions. This article is part of the theme issue ‘Conceptual challenges in microbial community ecology’.
Abstract Spatial self-organization is a hallmark of surface-associated microbial communities that is governed by local environmental conditions and further modified by interspecific interactions. Here, we hypothesize that spatial patterns of microbial cell-types can stabilize the composition of cross-feeding microbial communities under fluctuating environmental conditions. We tested this hypothesis by studying the growth and spatial self-organization of microbial co-cultures consisting of two metabolically interacting strains of the bacterium Pseudomonas stutzeri. We inoculated the co-cultures onto agar surfaces and allowed them to expand (i.e. range expansion) while fluctuating environmental conditions that alter the dependency between the two strains. We alternated between anoxic conditions that induce a mutualistic interaction and oxic conditions that induce a competitive interaction. We observed co-occurrence of both strains in rare and highly localized clusters (referred to as “spatial jackpot events”) that persist during environmental fluctuations. To resolve the underlying mechanisms for the emergence of spatial jackpot events, we used a mechanistic agent-based mathematical model that resolves growth and dispersal at the scale relevant to individual cells. While co-culture composition varied with the strength of the mutualistic interaction and across environmental fluctuations, the model provides insights into the formation of spatially resolved substrate landscapes with localized niches that support the co-occurrence of the two strains and secure co-culture function. This study highlights that in addition to spatial patterns that emerge in response to environmental fluctuations, localized spatial jackpot events ensure persistence of strains across dynamic conditions.
Denitrifying microbes sequentially reduce nitrate (NO 3 – ) to nitrite (NO 2 – ), NO, N 2 O, and N 2 through enzymes encoded by nar , nir , nor , and nos . Some denitrifiers maintain the whole four-gene pathway, but others possess partial pathways. Partial denitrifiers may evolve through metabolic specialization whereas complete denitrifiers may adapt toward greater metabolic flexibility in nitrogen oxide (NO x – ) utilization. Both exist within natural environments, but we lack an understanding of selective pressures driving the evolution toward each lifestyle. Here we investigate differences in growth rate, growth yield, denitrification dynamics, and the extent of intermediate metabolite accumulation under varying nutrient conditions between the model complete denitrifier Pseudomonas aeruginosa and a community of engineered specialists with deletions in the denitrification genes nar or nir . Our results in a mixed carbon medium indicate a growth rate vs. yield tradeoff between complete and partial denitrifiers, which varies with total nutrient availability and ratios of organic carbon to NO x – . We found that the cultures of both complete and partial denitrifiers accumulated nitrite and that the metabolic lifestyle coupled with nutrient conditions are responsible for the extent of nitrite accumulation.
Abstract Evidence suggests that bacterial community spatial organization affects their ecological function, yet details of the mechanisms that promote spatial patterns remain difficult to resolve experimentally. In contrast to bacterial communities in liquid cultures, surface-attached range expansion fosters genetic segregation of the growing population with preferential access to nutrients and reduced mechanical restrictions for cells at the expanding periphery. Here we elucidate how localized conditions in cross-feeding bacterial communities shape community spatial organization. We combine experiments with an individual based mathematical model to resolve how trophic dependencies affect localized growth rates and nucleate successful cell lineages. The model tracks individual cell lineages and attributes these with trophic dependencies that promote counterintuitive reproductive advantages and result in lasting influences on the community structure, and potentially, on its functioning. We examine persistence of lucky lineages in structured habitats where expansion is interrupted by physical obstacles to gain insights into patterns in porous domains.
