Biology subjects

Le Roux, F.

Publications and source records attributed to Le Roux, F..

7 recordsLinked to original sources

bioRxiv2025

Ecological constraints foster both extreme viral-host lineage stability and mobile element diversity in a marine community

Phages are typically viewed as very rapidly evolving biological entities. Little is known, however, about whether and how phages can establish long-term genetic stability. We addressed this eco-evolutionary question in an open marine animal associated system, through two longitudinal samplings years apart in an oyster farm, obtaining >1,000 virulent phages and >600 Vibrio crassostreae strains. Surprisingly, lineages of phage and bacteria were very persistent, with some phages remaining strictly identical after four years. The phage-vibrio infection network remained modular with multiple lineages co-habitating within individual oysters for long periods of time. Seasonal restriction of V. crassostreae, overwintering in wild oysters, and limited viral decay may explain phage stability. Oysters also act as hotspots of activity of diverse mobile genetic element (MGE), hosting plasmids, prophages, phage-plasmids and entirely new classes of satellite-plasmids. Our findings demonstrate how nested ecological constraints can stabilize viral lineages: oysters house vibrio populations that escape host immunity, vibrios restrict phages via receptors and defenses, and satellites parasitize their cognate helper phages. We suggest that ecological context can favor the long-term maintenance of viral lineages and stabilize MGE persistence in the ocean, even amid ongoing mutation and antagonistic co-evolution.

microbiology↗

bioRxiv2024

Generalists in a Specialist World: Vibrio-Phages with Broad Host Range

The host range of a bacteriophage--the diversity of hosts it can infect--is central to understanding phage ecology and applications. While most well-characterized phages have narrow host ranges, broad-host-range phages represent an intriguing component of marine ecosystems. The genetic and evolutionary mechanisms driving their generalism remain poorly understood. In this study, we analyzed Schizotequatroviruses and their Vibrio crassostreae hosts, collected from an oyster farm. Schizotequatroviruses exhibit broad host ranges, large genomes (~252 kbp) encoding 26 tRNAs, and conserved genomic organization interspersed with recombination hotspots. These recombination events, particularly in regions encoding receptor-binding proteins and antidefense systems, highlight their adaptability to host resistance. Notably, some lineages demonstrated receptor-switching between OmpK and LamB, showcasing their evolutionary flexibility. Despite their broad host range, Schizotequatroviruses were rare in the environment. Their scarcity could not be attributed to burst size, which was comparable to other phages in vitro, but may result from ecological constraints or fitness trade-offs, such as their preference for targeting generalist vibrios in seawater rather than the patho-phylotypes selected in oyster farms. Our findings clarify the genetic and ecological trade-offs shaping Schizotequatrovirus generalism and provide a foundation for future phage applications in aquaculture and beyond.

microbiology↗

bioRxiv2024

Sedentary chromosomal integrons as biobanks of bacterial anti-phage defence systems

Integrons are genetic systems that accelerate bacterial adaptation by acquiring and shuffling gene cassettes. Mobile integrons spread antibiotic resistance genes among bacteria, while the sedentary chromosomal integrons contain up to hundreds of cassettes of unknown function. Here, we show that many of these cassettes encode anti-phage defence systems. We found numerous streamlined variants of known systems, which have presumably evolved to fit the small size constraints of integron cassettes recombination and genesis. Intrigued by the rarity of known systems in the sedentary chromosomal integron of the Vibrio cholerae 7th cholera pandemic strain, we tested the presence of anti-phage functions in all its cassettes of unknown function. We found that at least 16 of the strain cassettes have an anti-phage activity in V. cholerae or E. coli. This represents 18% of the tested cassettes and almost 10% of all the integron cassettes, providing at long last a key adaptive role for a significant fraction of the sedentary integrons. Most of the newly discovered systems have little or no similarity to previously known ones and our experiments show that several mediate defence through cell lysis or growth arrest. One of these systems encodes a 64 amino acids protein, which represents the smallest known protein providing autonomous phage resistance. Given the thousands of uncharacterized integron cassette families, integrons could represent an untapped treasure trove of streamlined anti-phage systems.

genetics↗

bioRxiv2023

Phage inducible chromosomal minimalist island (PICMI), a family of satellites of marine virulent phages

Phage satellites are genetic elements that hijack the phage machinery for their own dissemination. However, only few phage satellites have been characterized, and mechanisms by which they influence microbial evolution in nature are unclear. Here we identify a new family of satellites, the Phage Inducible Chromosomal Minimalist Island (PICMI), which is broadly distributed in the marine bacteria Vibrionaceae. PICMI is characterized by reduced gene content, does not encode genes for capsid remodeling and packages its DNA as a concatemer. PICMI is integrated in the bacterial host genome at the end of the fis regulator and encodes three core proteins necessary for excision and replication. PICMI is dependent on virulent phage particles to spread to other bacteria and confers host protection from other competitive phages, without interfering with its helper phage. The discovery of PICMI strongly suggests that phages, including virulent ones, play important roles for mobility of phage defense elements.

microbiology↗

bioRxiv2023

Cooperation and cheating orchestrate Vibrio assemblages and polymicrobial synergy in oysters infected with OsHV-1 virus

Polymicrobial diseases significantly impact the health of humans and animals but remain understudied in natural systems. We recently described the Pacific Oyster Mortality Syndrome (POMS), a polymicrobial disease that impacts oyster production and is prevalent worldwide. Analysis of POMS-infected oysters on the French North Atlantic coast revealed that the disease involves co-infection with the endemic ostreid herpesvirus 1 (OsHV-1) and virulent bacterial species such as Vibrio crassostreae. However, it is unknown whether consistent Vibrio populations are associated with POMS in different regions, how Vibrio contribute to POMS, and how they interact with the OsHV-1 virus during pathogenesis. We resolved the Vibrio population structure in oysters from a Mediterranean ecosystem and investigated their functions in POMS development. We find that Vibrio harveyi and Vibrio rotiferianus are the predominant species found in OsHV-1-diseased oysters and show that OsHV-1 is necessary to reproduce the partition of the Vibrio community observed in the field. By characterizing the interspecific interactions between OsHV-1, V. harveyi and V. rotiferianus, we find that only V. harveyi synergizes with OsHV-1. When co-infected, OsHV-1 and V. harveyi behave cooperatively by promoting mutual growth and accelerating oyster death. V. harveyi showed high virulence potential in oysters and dampened host cellular defenses, making oysters a more favorable niche for microbe colonization. We next investigated the interactions underlying the co-occurrence of diverse Vibrio species in diseased oysters. We found that V. harveyi harbors genes responsible for the biosynthesis and uptake of a key siderophore called vibrioferrin. This important resource promotes the growth of V. rotiferianus, a cheater that efficiently colonizes oysters during POMS without costly investment in host manipulation nor metabolite sharing. By connecting field-based approaches, laboratory infection assays and functional genomics, we have uncovered a web of interdependencies that shape the structure and function of the POMS pathobiota. We showed that cooperative behaviors contribute to synergy between bacterial and viral co-infecting partners. Additional cheating behaviors further shape the polymicrobial consortium. Controlling such behaviors or countering their effects opens new avenues for mitigating polymicrobial diseases.

microbiology↗

bioRxiv2022

Divergence in bacterial ecology is reflected by difference in population genetic structure, phage-predator load and host range

Phages depend on their bacterial host to replicate, but how habitat, density and diversity of the host population drive phage ecology is not well understood. Here, we addressed this question by comparing two populations of marine bacteria and their phages collected during a time series sampling in an oyster farm. Vibrio crassostreae reproduces more specifically in oysters. This population is genetically structured into clades of near clonal strains favoring infection by closely related phages and leading to a modular structure of the phage-bacterial infection network. Vibrio chagasii, on the other hand, blooms in the water column from where it can colonize oysters via filter-feeding. We found higher phage predation pressure on V. chagasii that did not result from a broader host range of the phages but rather from a greater burst size generating more infectious particles in the environment. We showed that contrasting patterns of genetic diversity for host and phage lead to different infection network architectures. We also provided evidence that a bloom of phages generates epigenetic and genetic variability that can be selected to counteract host defense systems.

microbiology↗

bioRxiv2021

Genetic determinism of phage-bacteria coevolution in natural populations

Coevolution between bacteriophage (or phage) and their bacterial host is thought to be key for the coexistence of these antagonists. Recent studies have revealed the major role of mobile genetic elements in the emergence of phage resistant hosts but how phage escape these defenses in the wild remained to be explored. Here we show a striking parallel in phage evolving counter defenses to host defenses in natural population. We established a large collection of phages and their bacterial hosts and we explored the genetic structure of their interaction. We find that clearly delineated genomic clusters of phage are specific for distinct clades within a bacterial species, Vibrio crassostreae, yet while all phages can adsorb, only a subset of hosts are killed due to intracellular defense mechanisms. Host genomes contain multiple mobile defense genes and susceptibility to phage is negatively correlated with genome size. Phages also display extensive gene content variation, but their genome size remains conserved. We show that this gene content variation in hosts and phage is due to rapid turnover of genes involved in defense and escape, and that by exchanging anti-defense genes, phages irreversibly switch host. This could be indicative of co-evolution following the matching-allele-model of specificity and the spatial and temporal variability of phage infectivity further suggests that negative-frequency dependent selection drives phage-vibrio coevolutionary dynamics. We propose a "pan-escape system" that can be shared among phages by homologous recombination within a population that infects a bacterial host.

microbiology↗