A mechanistic approach to understand microbiome-viriome dynamics in nature

Project Information

DYNAMIC

Grant agreement ID: 884988

DOI

10.3030/884988

Project closed

EC signature date 5 May 2020

Start date 1 January 2021

End date 31 December 2023

Funded under

• EXCELLENT SCIENCE - European Research Council (ERC)

Total cost

€ 1 886 516,25

EU contribution

€ 1 886 516,25

Coordinated by

INSTITUT FRANCAIS DE RECHERCHE POUR L'EXPLOITATION DE LA MER
France

Periodic Reporting for period 2 - DYNAMIC (A mechanistic approach to understand microbiome-viriome dynamics in nature)

Reporting period: 2022-07-01 to 2023-12-31

Summary of the context and overall objectives of the project

This project aimed to explore the potential of phages, natural predators of bacteria, in regulating bacterial populations in farming systems like aquaculture. Specifically, the study investigated how phages control the abundance and diversity of bacteria, such as oyster pathogenic vibrios, in a natural setting like an oyster farm. The researchers assembled a comprehensive collection of fully sequenced phages and their vibrio hosts, sampled at high temporal resolution. Contrary to expectations, they found a certain degree of stability in the system, with consistent clades of bacteria and phage genera across various samplings. Spatial and temporal patterns in phage populations aligned with their bacterial hosts, confirming the role of phages in vibrio ecology. Quantitative tests revealed modular and nested phage infection networks, distinguishing between generalist and specialist phages. Genome analyses identified genetic alterations in both host and phage lineages, indicating defense and counter-defense mechanisms. Evolutionary scenarios involving receptor mutations, gene gain and loss together with changes in phage sensitivity were observed. The study validated observations from more simplified models and emphasized the importance of gene transfer in coevolution. Overall, the research highlights the practical applications of understanding phage-bacteria dynamics in farming practices.

Work performed from the beginning of the project to the end of the period covered by the report and main results achieved so far

The project investigates molecular mechanisms and evolutionary dynamics in bacteria-phage interactions in natural environments. Several publications explore these dynamics, focusing on factors like local adaptation, phage defense mechanisms, phage counter defenses and host population structures. Discoveries led to a reassessment of experimental design, resulting in a new time-series sampling project at an oyster farm. This effort yielded extensive datasets of >1200 phages and 600 Vibrio crassostreae isolates. Further analysis identified a new family of satellites, Phage-Inducible Chromosomal Minimalist Islands (PICMIs), that hitchhikes a virulent phage and influences host defense. Schizotequatroviruses, the broader host range phages, exhibited an extended latency period and reduced burst size, consistent with the "cost of generalism" theory. Moreover, the study identified phage lineages evolving through receptor mutations, impacting host range and potentially virulence. Overall, the research provides a comprehensive analysis of virome dynamics in oyster farms, shedding light on complex phage-host interactions.

Progress beyond the state of the art and expected potential impact (including the socio-economic impact and the wider societal implications of the project so far)

The project explores co-evolution dynamics between phages and bacteria using an innovative phenotypic experimental strategy, revealing surprising stability within vibrio and phage components despite vast genetic diversity. Genome analyses highlight genetic convergence in specific phage lineages, suggesting novel mechanisms of phage adaptation. The discovery of numerous satellites in Vibrionaceae genomes, including PICMIs, unveils their role in shaping bacterial evolution. Ongoing efforts aim to understand the functions and attributes of satellites, including their activation mechanisms and impact on host resistance.

Outstanding question addressed in the present project