Biotic Interactions Are More Important than Propagule Pressure in Microbial Community Invasions

Abstract

Microbial probiotics are intended to improve functions in diverse ecosystems, yet probiotics often fail to establish in a preexisting microbiome. This is a species invasion problem. The relative importance of the two major factors controlling establishment in this context—propagule pressure (inoculation dose and frequency) and biotic interactions (composition of introduced and resident communities)—is unknown. We tested the effect of these factors in driving microbial composition and functioning following 12 microbial community invasions (e.g., introductions of many microbial invaders) in microcosms. Ecosystem functioning over a 30-day postinvasion period was assessed by measuring activity (respiration) and environment modification (dissolved organic carbon abundance). To test the dependence on environmental context, experiments were performed in two resource environments. In both environments, biotic interactions were more important than propagule pressure in driving microbial composition and community function, but the magnitude of effect varied by environment. Successful invaders comprised approximately 8% of the total number of operational taxonomic units (OTUs). Bacteria were better invaders than fungi, with average relative abundances of 7.4% ± 6.8% and 1.5% ± 1.4% of OTUs, respectively. Common bacterial invaders were associated with stress response traits. The most resilient bacterial and fungal families, in other words, those least impacted by invasions, were linked to antimicrobial resistance or production traits. Illuminating the principles that determine community composition and functioning following microbial invasions is key to efficient community engineering. IMPORTANCE With increasing frequency, humans are introducing new microbes into preexisting microbiomes to alter functioning. Example applications include modification of microflora in human guts for better health and those of soil for food security and/or climate management. Probiotic applications are often approached as trial-and-error endeavors and have mixed outcomes. We propose that increased success in microbiome engineering may be achieved with a better understanding of microbial invasions. We conducted a microbial community invasion experiment to test the relative importance of propagule pressure and biotic interactions in driving microbial community composition and ecosystem functioning in microcosms. We found that biotic interactions were more important than propagule pressure in determining the impact of microbial invasions. Furthermore, the principles for community engineering vary among organismal groups (bacteria versus fungi).

The role of competition versus cooperation in microbial community coalescence

“…While this assumption may be sensible in some cases [45], it is an oversimplification in others [31]. Extending this theoretical framework to study the effects of resource supply variation, e.g., by allowing substrate diversification from a single supplied resource [6,7], is a promising direction for future research.…”

“…Ignoring environmental fluctuations allowed us to focus on coalescence outcomes in terms of the species interaction structure alone. While this assumption may be sensible in some cases [47], it is an oversimplification in others [33]. Therefore, studying the complex interplay between biotic interactions and environmental factors, e.g., by allowing substrate diversification from a single supplied resource [6, 7], or perturbing the supply vector periodically to simulate some form of seasonality, is a promising direction for future research.…”

“…These cross-feeding networks can vary in their particular link distribution (the architecture of the flow of metabolites shared across species), but also in their link weights (the fraction of consumed resources that is secreted to the environment as metabolic by-products instead of kept for private consumption) [30]. Indeed, several studies have suggested that a combination of competitive and cooperative interactions may determine the outcome of coalescence in microbial communities [31][32][33].…”

“…Yet, these microbial September 3, 2021 2/19 communities exhibit cooperation through a typically dense cross-feeding network, where leaked metabolic by-products of one species are shared as public goods across the entire community [29][30][31]. Indeed, several studies have suggested that a combination of competitive and cooperative interactions may determine the outcome of coalescence in microbial communities [21,32,33].…”

“…Considering only biotic perturbations allowed us to pinpoint the effect of each interaction separately. While this assumption may be sensible in some cases [50], it surely is oversimplifying in others [33]. When two communities collide, the process will entail, in general, a mixture of biotic and abiotic perturbations.…”