Invasion in microbial communities: Role of community composition and assembly processes

Marta Kinnunen

Research output: Book/ReportPh.D. thesis

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Abstract

Microbes contribute to all biogeochemical cycles on earth and are responsible for key biological processes that support the survival of plants and animals. There is increased interest in controlling and managing microbial communities in different ecosystems in order to make targeted microbiological processes more effective. In order to manage microbial communities, it is essential to understand the factors that shape and influence microbial community composition. In addition to abiotic factors, such as environmental conditions and resource availability, biotic factors also shape the dynamics of microbial community assembly. Biotic factors include interactions between different microbial groups as well as the community response to alien species – invaders.
Microbial invasions can have significant effects on the composition and functioning of resident communities. There is, however, lack of agreement on the core determinants of invasion in microbial communities. Current models and concepts for invasion in microbial ecology are largely based on the macro-ecology literature. Although attempts have been made to examine the applicability of these concepts to microbial communities, a general conceptual framework for microbial invasion applicable across ecosystems is missing. The overall aim of this PhD project was therefore to propose a conceptual framework to study microbial community invasion and to test this framework against experimental observations.
Based on a synthesis of earlier frameworks on invasion and community ecology, I defined invasion in a microbial community as the establishment of an alien microbial type in a resident community and have proposed simple criteria to define aliens, residents, and alien establishment, applicable across a wide variety of communities. I suggested the adoption of the community ecology framework advanced by Vellend (2010) to identify determinants of invasion. This framework lists the four fundamental processes that govern community assembly as: dispersal, selection, drift and diversification. We have suggested that it is important to determine which processes dominate the assembly of a resident community in order to understand what governs invasion in that community.
To test invasion in microbial communities while controlling the processes driving community assembly, I developed a high-throughput flow-through experimental microcosm system that enabled me to manipulate the relative importance of selection versus drift during initial community assembly. I used this new system to establish resident microbial biofilm communities dominated by nitrite-oxidizing bacteria, where the direction of selection as well as contribution of drift was manipulated through differential nitrite loading rates.
Subsequently, I experimentally characterized the community assembly processes in the biofilm communities, using replicate communities assembled under same conditions. Both total community and guild-level analyses provided evidence for contribution of neutral processes (drift) combined with selection. More precisely, I observed the deterministic enrichment of certain types of nitrite-oxidizing bacteria in the biofilms: elevated nitrite loading selected for a single Nitrotoga representative, while lower nitrite conditions selected for a number of Nitrospira.
I then repeated the assembly experiment and subjected the assembled biofilms to invasion by a Nitrotoga HW29 culture. I found no significant (negative) correlation between community diversity and invasion success, in contrast with the often cited diversity/invasibility relationship. Instead, I observed that at high phylogenetic similarity between invader and resident types, the effect of selection is surpassed by the effect of drift on invasion success. My results suggest that controlling invasion in communities that contain members that are phylogenetically similar to the invader is nearly impossible because stochastic processes determine the invasion outcome when selection towards invader and resident community is similar.
In conclusion, during this PhD project I proposed a simple conceptual framework to study and characterize microbial invasions. This conceptual framework allows comparison of experimental observations across ecosystems using a coherent ecological terminology and consideration of community assembly processes rather than indices to describe community composition. Furthermore, I experimentally identified the dominant processes in newly assembled biofilms enriched in nitrite-oxidizing guilds before subjecting the resident guilds to invasion by an alien nitrite-oxidizer. The results of my experiments indicate that neutral processes have significantly higher contribution to community assembly – including invasion – than previously suggested.
Original languageEnglish
Place of PublicationKgs. Lyngby
PublisherDepartment of Environmental Engineering, Technical University of Denmark (DTU)
Number of pages46
Publication statusPublished - 2017

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