Historical contingencies and phage induction diversify bacterioplankton communities at the microscale

Abstract

In many natural environments, microorganisms decompose microscale resource patches made of complex organic matter. The growth and collapse of populations on these resource patches unfold within spatial ranges of a few hundred micrometers or less, making such microscale ecosystems hotspots of heterotrophic metabolism. Despite the potential importance of patch-level dynamics for the large-scale functioning of heterotrophic microbial communities, we have not yet been able to delineate the ecological processes that control natural populations at the microscale. Here, we address this challenge by characterizing the natural marine communities that assembled on over 1,000 individual microscale particles of chitin, the most abundant marine polysaccharide. Using low-template shotgun metagenomics and imaging, we find significant variation in microscale community composition despite the similarity in initial species pools across replicates. Chitin-degrading taxa that were rare in seawater established large populations on a subset of particles, resulting in a wide range of predicted chitinolytic abilities and biomass at the level of individual particles. We show, through a mathematical model, that this variability can be attributed to stochastic colonization and historical contingencies affecting the tempo of growth on particles. We find evidence that one biological process leading to such noisy growth across particles is differential predation by temperate bacteriophages of chitin-degrading strains, the keystone members of the community. Thus, initial stochasticity in assembly states on individual particles, amplified through ecological interactions, may have significant consequences for the diversity and functionality of systems of microscale patches.

Insights into community assembly mechanisms, biogeography, and metabolic potential of particle-associated and free-living prokaryotes in tropical oligotrophic surface oceans

“…Moreover, our study supports previous observations (Jain et al, 2021) that the relative influence of HoS is higher in FL assemblages than in their PA counterparts. Particularly, previous studies have indicated that individual particles differed in colonizing communities (Bizǐc-Ionescu et al, 2018;Szabo et al, 2022), whereas HeS can poorly explain the community turnover of PA communities in our study. This result may be explained by the fact that the PA assemblages in this study were collected from the upper oligotrophic oceans, where changes in PA communities related to carbon availability may be much slower due to constant supply of labile, easily degradable organic matter (Bizǐc-Ionescu et al, 2018).…”

Annotation-free discovery of functional groups in microbial communities

“…during the colonization of a new environment, environmental filters couple the dynamics of functionally equivalent species 32 . In contrast, as community composition approaches a steady state, functional group members can be decoupled by various factors, including historical contingencies, different sensitivities to environmental parameters (O2 concentration), and biotic interactions, to name a few 33 . It is in this scenario, where the community composition is not undergoing early successional changes, that approaches such as ours can be applied.…”

Formation and emergent dynamics of spatially organized microbial systems

“…New experimental approaches are slowly deciphering the colonization dynamics of nutrient-rich surfaces. For example, colonization of marine snow is mimicked with the use of magnetic beads that are covered with nutritious substrate and that can be readily extracted from aqueous media [ 34 , 35 ]. This has revealed stochastic effects on population dynamics during the early stages of colonization, arising from both the attachment process [ 34 ] and viral lysis [ 35 ].…”

“…For example, colonization of marine snow is mimicked with the use of magnetic beads that are covered with nutritious substrate and that can be readily extracted from aqueous media [ 34 , 35 ]. This has revealed stochastic effects on population dynamics during the early stages of colonization, arising from both the attachment process [ 34 ] and viral lysis [ 35 ]. In terms of attachment success, theoretical studies suggest that motility can be a key factor in colonization of surfaces in aquatic environments, as motile bacteria are expected to have two to four orders of magnitude higher diffusion coefficients than non-motile cells, and therefore increased particle encounter rates [ 36 ].…”