Determining causal links between interaction type and network structure in microbial communities

Lead Research Organisation: UNIVERSITY OF EXETER
Department Name: Biosciences

Abstract

Ecological communities exist as networks of interacting species, and the structure of these networks determine their stability and function. Observational studies suggest that network structure depends upon whether interactions between species are predominantly mutualistic or antagonistic, however the causality of this relationship remains unclear. Here, we will use communities of bacteria and their symbiotic plasmids to experimentally determine how interaction type (mutualistic versus antagonistic) affects community network structure. Our system is ideal to address these questions because bacteria-plasmid interactions can be switched from antagonistic to mutualistic through simple environmental manipulations (the addition of antibiotics to which the plasmids confer resistance), and changes in community network structure can be observed over a matter of weeks. The large-scale of this project is made possible by the application of a novel culture-free method, epicPCR, which allows high-throughput assessment of bacteria-plasmid associations. The predicted role of ecological stability, as well as novel eco-evolutionary mechanisms, underpinning the interaction type-network structure relationships will be assessed by a combination of phenotypic and genetic experiments complemented by theory.

Planned Impact

The proposed work will unambiguously determine whether different types of interactions (positive or negative) within ecological communities can determine the structure and stability of ecological networks. We have identified four groups (in addition to academics) of potential beneficiaries

1. Biotechnology industry
Microbial communities are used in a range of applied contexts, including the remediation of pollutants. Frequently, the ability to tolerate toxins and break down pollutants relies on genes encoded by plasmids. The structure of microbial networks determines the extent that these beneficial plasmids spread through microbial communities, and create opportunities for environmental manipulation of communities to maximize their effectiveness at remediation. We will seek to develop existing (e.g. the mining consultant Wardell Armstrong), and establish new partnerships with UK companies to apply the results from this project to achieve societal and commercial benefits. This will involve working closely with the University of Exeter IIB to establish new contacts and attending workshops. Milestones will be the establishment of CASE partnerrhips.

2. Clinicians
As well as conferring traits that are beneficial, plasmids are also responsible for one of the major threats to human health: antibiotic resistance genes. Microbial networks structure could play a major role in their spread. We will continue to engage with our key clinical collaborators in Switzerland and Denmark. Both work closely with patients with cystic fibroses, a condition whereby patients are chronically infected with a community of opportunistic bacterial pathogens. Management of antibiotic resistance in this context is critical, and it is likely that manipulation of bacteria-plasmid networks will play an important role. The main milestone will therefore be reporting of our results and success will be measured by these results leading to clinical studies of bacteria-plasmid networks and how they can be manipulated. We will also seek new links with clinicians working with opportunistic bacterial infections and dysbioses, with assistance both from IIB staff and the National Institute for Health Research (NIHR) Collaboration for Leadership in Applied Health Research and Care (CLAHRC) South West Peninsula (PenCLAHRC). Establishing new clinical collaborators will be our milestones, while developing new potential clinical applications will be our measure of success.

3. Soil stakeholders
The focus on microbial community structure and the spread of antibiotic resistance in soil has direct relevance to a wide range of individuals and organisations related to agriculture and ecosystem services, including farmers; retailers and agri-enterprises; and Government agencies, policy makers and NGOs related to agriculture and ecosystem services (e.g. Natural England, Defra). We will engage directly with these groups, emphasizing the potentially key role of microbial network structure, by taking advantage of existing workshops to which these stakeholders will attend, and arrnaging a half day workshop coinciding with a project meeting of all investigators and collaborators where local stakeholders and academics will be invited. Participating at these workshops will be our milestones for this activity, with success measured by the establishing new collaborations and potential applications to minimising antibiotic resistance in soil.

4. Public
We have experience of successfully engaging the public and media with our previous projects, which we will draw on in undertaking the following activities: engagement with popular science magazines; social media; school lectures; participation in ongoing University of Exeter piblci engagement events.

Publications

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Brockhurst M (2022) Ecological and evolutionary solutions to the plasmid paradox in Trends in Microbiology

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Newbury A (2022) Fitness effects of plasmids shape the structure of bacteria-plasmid interaction networks. in Proceedings of the National Academy of Sciences of the United States of America

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Castledine M (2022) Greater Phage Genotypic Diversity Constrains Arms-Race Coevolution. in Frontiers in cellular and infection microbiology

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Sanders D (2023) How artificial light at night may rewire ecological networks: concepts and models in Philosophical Transactions of the Royal Society B: Biological Sciences

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Dimitriu T (2021) Increased copy number couples the evolution of plasmid horizontal transmission and plasmid-encoded antibiotic resistance. in Proceedings of the National Academy of Sciences of the United States of America

 
Description interaction between bacteria and their symbionts greatly affects evolution
Exploitation Route Led to an independent BBSRc fellowship and inspired others to take similar approaches
Sectors Environment

Manufacturing

including Industrial Biotechology

 
Title Collection of studies included in the review from How artificial light at night may rewire ecological networks: concepts and models 
Description Artificial light at night (ALAN) is eroding natural light cycles thereby changing species distributions and activity patterns. Yet, little is known about how ecological interaction networks respond to this global change driver. Here, we assess the scientific basis of the current understanding of community-wide ALAN impacts. Based on current knowledge, we conceptualize and review four major pathways by which ALAN may affect ecological interaction networks by (i) impacting primary production, (ii) acting as an environmental filter affecting species survival, (iii) driving the movement and distribution of species, and (iv) changing functional roles and niches by affecting activity patterns. Using an allometric-trophic network model, we then test how a shift in temporal activity patterns for diurnal, nocturnal, and crepuscular species impacts food web stability. The results indicate that diel niche shifts can severely impact community persistence by altering the temporal overlap between species, which leads to changes in interaction strengths and rewiring of networks. ALAN can thereby lead to biodiversity loss through the homogenization of temporal niches. This integrative framework aims to advance a predictive understanding of community-level and ecological-network consequences of ALAN and their cascading effects on ecosystem functioning.This article is part of the theme issue 'Light pollution in complex ecological systems'. 
Type Of Material Database/Collection of data 
Year Produced 2023 
Provided To Others? Yes  
URL https://rs.figshare.com/articles/dataset/Collection_of_studies_included_in_the_review_from_How_artif...
 
Title Collection of studies included in the review from How artificial light at night may rewire ecological networks: concepts and models 
Description Artificial light at night (ALAN) is eroding natural light cycles thereby changing species distributions and activity patterns. Yet, little is known about how ecological interaction networks respond to this global change driver. Here, we assess the scientific basis of the current understanding of community-wide ALAN impacts. Based on current knowledge, we conceptualize and review four major pathways by which ALAN may affect ecological interaction networks by (i) impacting primary production, (ii) acting as an environmental filter affecting species survival, (iii) driving the movement and distribution of species, and (iv) changing functional roles and niches by affecting activity patterns. Using an allometric-trophic network model, we then test how a shift in temporal activity patterns for diurnal, nocturnal, and crepuscular species impacts food web stability. The results indicate that diel niche shifts can severely impact community persistence by altering the temporal overlap between species, which leads to changes in interaction strengths and rewiring of networks. ALAN can thereby lead to biodiversity loss through the homogenization of temporal niches. This integrative framework aims to advance a predictive understanding of community-level and ecological-network consequences of ALAN and their cascading effects on ecosystem functioning.This article is part of the theme issue 'Light pollution in complex ecological systems'. 
Type Of Material Database/Collection of data 
Year Produced 2023 
Provided To Others? Yes  
URL https://rs.figshare.com/articles/dataset/Collection_of_studies_included_in_the_review_from_How_artif...
 
Title Data and Models (version 1) 
Description This archive contains the following: a) Phage Susceptibility - a folder containing the scripts and data for MCMCglmms investigating the role of host phylogeny in the susceptibility of Staphylococcus to a bacteriophage, ISP. b) Leave One Out Cross Validation - a folder containing the scripts and data for MCMCglmm leave-one-out cross-validation where the ability of the model to predict the susceptibility of an unknown host based on the susceptibility of its neighbours and their phylogenetic relatedness is tested. The complete phylogeny for the 64 Staphylococcus strains can be found in either folder and is called: Staph_Phylogeny.nwk 
Type Of Material Database/Collection of data 
Year Produced 2022 
Provided To Others? Yes  
URL https://figshare.com/articles/dataset/Data_and_Models_version_1_/21642209