Niche and neutral processes in aquatic bacterial communities: Are all things equal?

Abstract

Understanding the mechanisms that generate and regulate bacterial biodiversity is a key focus of microbial ecology. Indeed, understanding how bacterial communities will respond to varying environmental stressors, pollution and anthropogenic climate change has important consequences for humanity, ecosystem health and function. Species sorting (i.e., deterministic environmental selection) has been proposed as one of the major processes involved in regulating bacterial community composition. However, with the development of the Neutral Theory of Biodiversity and Biogeography, the importance of neutral processes (i.e., random births, deaths, migration and speciation events) has become increasingly recognised as influencing community structure in a range of different ecological communities and habitats. Consequently, to what extent are bacterial communities assembled by stochastic neutral processes as opposed to deterministic species sorting? In order to address this question, I investigated aquatic bacterial communities using hypothesis-driven field studies, mesocosm and microcosm experiments utilising automated ribosomal intergenic spacer analysis (ARISA) and 454 pyrosequencing of 16S rRNA genes. Here, I present evidence suggesting that both niche and neutral processes are important in structuring bacterial communities, although the latter appeared to increase when bacterial migration was prohibited or when strong selection pressures were observed. For example, the neutral model of Sloan et al. (2006) explained a fair portion (30-65%) of the variation in the field investigations, and the immigration parameters of Etienne’s (2005) neutral model responded to different immigration times in a controlled microcosm experiment. However, when a closed system was investigated (i.e., where no bacterial immigration was allowed), with larger environmental stressors, species sorting was confirmed to be of clear importance for the structure of aquatic bacterial communities. Species sorting, and other niche processes, are undoubtedly important regulators of bacterial community structure, but the role of stochastic neutral processes should not be ignored, particularly during the early stages of community development. As well as studying species sorting and neutral processes, I investigated other macroecological patterns occurring within the microbial world predicted by both of these theoretical frameworks, viz: the taxon-area relationship (TAR), distance-decay and the taxon-time relationship (TTR). The TAR, which predicts an increase in taxon richness with increased habitat size, is a ubiquitous ecological pattern observed among macroorganisms and is a cornerstone concept of macroecology. However, it is still relatively unknown as to whether positive TARs are observed in the microbial world; let alone if they are ubiquitous. Indeed, the occurrence of positive TARs and distance-decay relationships are predicted by both neutral theory and species sorting processes, but for two very different reasons.

Here, I present a controlled and replicated empirical evaluation of the TAR in bacterial communities using aquatic mesocosms that ranged from 0.25 – 550 L in volume. Using high-throughput 454 pyrosequencing and ARISA, I provide no evidence of a positive TAR in these aquatic bacterial communities. In fact, a significant negative TAR was identified, with physicochemical parameters (DO% and TOC) explaining the majority of the variation in taxon richness. Evidence of bacterial succession was also observed, whereby bacterial communities became more dissimilar to each other over time and a positive TTR was identified. Although patterns of distance-decay were observed in this study, the results were not unequivocal and the relationship appeared to depend on the spatial scale of observation. This project provides evidence of a range of macroecological processes occurring within the microbial world and contributes significant knowledge regarding the assembly, structure and diversity of aquatic bacterial communities.