A Small Number of Phylogenetically Distinct Clonal Complexes Dominate a Coastal Vibrio cholerae Population

Abstract

Vibrio cholerae is a ubiquitous aquatic microbe in temperate and tropical coastal areas. It is a diverse species, with many isolates that are harmless to humans, while others are highly pathogenic. Most notable among them are strains belonging to the pandemic O1/O139 serogroup lineage, which contains the causative agents of cholera. The environmental selective regimes that led to this diversity are key to understanding how pathogens evolve in environmental reservoirs. A local population of V. cholerae and its close relative Vibrio metoecus from a coastal pond and lagoon system was extensively sampled during two consecutive months across four size fractions (480 isolates). In stark contrast to previous studies, the observed population was highly clonal, with 60% of V. cholerae isolates falling into one of five clonal complexes, which varied in abundance in the short temporal scale sampled. V. cholerae clonal complexes had significantly different distributions across size fractions and the two environments sampled, the pond and the lagoon. Sequencing the genomes of 20 isolates representing these five V. cholerae clonal complexes revealed different evolutionary trajectories, with considerable variations in gene content with potential ecological significance. Showing genotypic differentiation and differential spatial distribution, the dominant clonal complexes are likely ecologically divergent. Temporal variation in the relative abundance of these complexes suggests that transient blooms of specific clones could dominate local diversity. IMPORTANCEVibrio cholerae is commonly found in coastal areas worldwide, with only a single group of this bacterium capable of causing severe cholera outbreaks. However, the potential to evolve the ability to cause disease exists in many strains of this species in its aquatic reservoir. Understanding how pathogenic bacteria evolve requires the study of their natural environments. By extensive sampling in a geographically restricted location in the United States, we found that most cells of a V. cholerae population belong to only a small number of strains. Analysis of their genome composition and spatial distribution indicates differential environmental adaptations between these strains. Other strains exist in smaller numbers, and the population was found to be temporally varied. This suggests frequent bloom and collapse cycles on a time scale of weeks. These population dynamics make it possible that more virulent strains could stochastically rise to large numbers, allowing for infection to occur. W hile long thought of as being specifically adapted to life as a pathogen in the human gut (1), numerous strains of Vibrio cholerae with varied degrees of virulence thrive in the brackish waters of lagoons and estuaries of the world (2), from the coast of Australia (3) to Iceland (4). The bacterium is believed to form close associations with aquatic invertebrates, preferentially living a life attached to the chitinous surfaces of those animals (5, 6). It is also regularly isolated f...

Fish as Hosts of Vibrio cholerae

“…Non-O1/non-O139 V. cholerae serogroups are also linked to V. cholerae gastroenteritis as well as to wound infections and bacteremia (Deshayes et al, 2015 ). V. cholerae O1, O139 and non-O1/O139 comprise a single taxonomic species and their habitats attributes are similar (Lewin, 1996 ), however, recently it has been suggested that not all strains of V. cholerae species share the same niche (Kirchberger et al, 2016 ). The role of CT in the environment is not understood.…”

Sequential displacement of Type VI Secretion System effector genes leads to evolution of diverse immunity gene arrays in Vibrio cholerae

“…Numerous mostly harmless lineages of Vibrio coexist within niches, competing for largely similar resources2. Among them are a few human pathogens of relevance, including Vibrio cholerae, the causative agent of the sometimes dramatic and lethal cholera diarrhea.…”

Environmental vibrios represent a source of antagonistic compounds that inhibit pathogenic Vibrio cholerae and Vibrio parahaemolyticus strains

“…Nucleotide analysis confirmed that all strains were Vibrio isolates using a criteria with a 99%–100% query coverage and an E ‐value of 0. The hsp60 locus was chosen for phylogenetic analysis since it has previously been used to characterize the population‐level diversity of vibrios and provides a robust and more defined tree structure compared to the 16S rRNA gene (Cordero, Wildschutte, et al., ; Hunt et al., ; Kirchberger et al., ; Preheim et al., ). From phylogenetic results, we identified that 40 of the 102 strains were unique at hsp60 nucleotide sequence.…”