Abstract

Understanding how microbial traits affect the evolution and functioning of microbial communities is fundamental for improving the management of harmful microorganisms, while promoting those that are beneficial. Decades of evolutionary ecology research has focused on examining microbial cooperation, diversity, productivity and virulence but with one crucial limitation. The traits under consideration, such as public good production and resistance to antibiotics or predation, are often assumed to act in isolation. Yet, in reality, multiple traits frequently interact, which can lead to unexpected and undesired outcomes for the health of macroorganisms and ecosystem functioning. This is because many predictions generated in a single-trait context aimed at promoting diversity, reducing virulence or controlling antibiotic resistance can fail for systems where multiple traits interact. Here, we provide a much needed discussion and synthesis of the most recent research to reveal the widespread and diverse nature of multi-trait interactions and their consequences for predicting and controlling microbial community dynamics. Importantly, we argue that synthetic microbial communities and multi-trait mathematical models are powerful tools for managing the beneficial and detrimental impacts of microbial communities, such that past mistakes, like those made regarding the stewardship of antimicrobials, are not repeated.

Highlights

  • Microorganisms exist and interact within complex and diverse communities (Cordero & Polz, 2014), where they play key roles in processes both beneficial and detrimental to humanity and the environment

  • There is a growing body of empirical work showing that predictions generated in a single-­trait context aimed at increasing diversity and stability, reducing virulence or controlling antibiotic resistance can fail for systems where multiple traits interact

  • Antibiotic resistance is a trait possessed by microbes whose population stability or productivity is greater than susceptible microbes in the presence of the relevant antimicrobial

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Summary

INTRODUCTION

Microorganisms exist and interact within complex and diverse communities (Cordero & Polz, 2014), where they play key roles in processes both beneficial and detrimental to humanity and the environment. Researchers have identified key pathogen traits that contribute towards virulence, such as cell-­surface appendages and secreted products that facilitate infection (Craig et al, 2004; Haiko & Westerlund-­Wikström, 2013; Dal Peraro & Van Der Goot, 2016), and have revealed key metabolic traits for metabolising complex carbohydrates in terrestrial and marine habitats (Grondin et al, 2017) and the gut microbiota (Cuskin et al, 2015) Identification of these traits has developed our understanding of processes within MCs. For instance, non-­ producers of cooperative secreted products, termed public goods, can reduce the stability, productivity and virulence of the microbial population (Lindsay et al, 2019; Özkaya et al, 2018; Popat et al, 2017; Sanchez & Gore, 2013). This is critical for promoting the beneficial functions that microbes provide and for successfully managing infectious diseases

HOW DO INTERACTING TRAITS AFFECT MICROBIAL COOPERATION?
Multiple interacting public goods
Multiple functions of public goods
Public good interactions with private traits
Interactions between cooperation types
The influence of public goods and interacting traits on productivity
Pyoverdine receptor
PG PG
Available resources Microbial competitors
Resistance to predation and competitive ability
Interacting traits during disease treatments
Secondary private trait
Response to social cues
Interspecific compeƟƟve ability
UpregulaƟon of other virulence factors
IMPLICATIONS AND FUTURE DIRECTIONS
AU THORSHIP

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