Associations and dynamics of Vibrionaceae in the environment, from the genus to the population level

Abstract

The Vibrionaceae, which encompasses several potential pathogens, including V. cholerae, the causative agent of cholera, and V. vulnificus, the deadliest seafood-borne pathogen, are a well-studied family of marine bacteria that thrive in a diverse habitats. To elucidate the environmental conditions under which vibrios proliferate, numerous studies have examined correlations with bulk environmental variables-e.g., temperature, salinity, nitrogen, and phosphate-and association with potential host organisms. However, how meaningful these environmental associations are remains unclear because data are fragmented across studies with variable sampling and analysis methods. Here, we synthesize findings about Vibrio correlations and physical associations using a framework of increasingly fine environmental and taxonomic scales, to better understand their dynamics in the wild. We first conduct a meta-analysis to determine trends with respect to bulk water environmental variables, and find that while temperature and salinity are generally strongly predictive correlates, other parameters are inconsistent and overall patterns depend on taxonomic resolution. Based on the hypothesis that dynamics may better correlate with more narrowly defined niches, we review evidence for specific association with plants, algae, zooplankton, and animals. We find that Vibrio are attached to many organisms, though evidence for enrichment compared to the water column is often lacking. Additionally, contrary to the notion that they flourish predominantly while attached, Vibrio can have, at least temporarily, a free-living lifestyle and even engage in massive blooms. Fine-scale sampling from the water column has enabled identification of such lifestyle preferences for ecologically cohesive populations, and future efforts will benefit from similar analysis at fine genetic and environmental sampling scales to describe the conditions, habitats, and resources shaping Vibrio dynamics.

Keywords: Vibrio; attachment; ecology; environmental correlation; niche; planktonic; population.

Figure 1

An overview of regression analyses indicate that temperature and salinity explain most variation in bulk-water total Vibrio abundance. The R², or pseudo-R², values associated with regression analyses are shown for selected environmental variables that are well-represented across studies. An individual study may perform multiple analyses because variables are considered for correlation independently (for ex. Wetz et al., 2008); because datasets are split (e.g., between seasons in Oberbeckmann et al., 2012); or because different sets of variables are considered sequentially (e.g., two variables versus six variables in the two All Seasons models from Froelich et al., 2013). Dots indicate bar heights, and where a dot occurs without a bar, R² was non-significant (i.e., R² = 0). Variables may have been log or exponentially transformed in references.

Figure 2

Variation in V. cholerae abundance or percent positive samples is best explained by temperature, other organisms, and salinity. R², or pseudo-R², values from analyses across studies are depicted grouped by variable, and then in rank order, with their associated reference. A reference may conduct multiple analyses for a given variable (e.g., on subsets of data or considering different variables combinations for data regression). Dots indicate bar heights, and where a dot occurs without a bar, R² was non-significant (i.e., R² = 0).

Figure 3

Variation in V. parahaemolyticus abundance or percent positive samples is best explained by temperature and other organisms. R², or pseudo-R², values from analyses across studies are depicted grouped by variable, and then in rank order, with their associated reference. A reference may conduct multiple analyses for a given variable (e.g., on subsets of data or considering different variables combinations for data regression). Dots indicate bar heights, and where a dot occurs without a bar, R² was non-significant (i.e., R² = 0).

Figure 4

Variation in V. vulnificus abundance or percent positive samples is best explained by temperature, and other organisms, including Vibrio. R², or pseudo-R², values from analyses across studies are depicted grouped by variable, and then in rank order, with their associated reference. A reference may conduct multiple analyses for a given variable (e.g., on subsets of data or considering different variables combinations for data regression). Dots indicate bar heights, and where a dot occurs without a bar, R² was non-significant (i.e., R² = 0).

Figure 5

V. cholerae favors lower salinity and occupies a broad temperature range. V. cholerae concentrations, i.e., MPN-estimated CFU or molecular marker gene copies per 100 mL, reported in different studies are plotted against the temperature (°C) and salinity values (ppt or psu) at which they were found. All studies report V. cholerae, including O1/O139 and non-O1/non-O139, except for Heidelberg et al. (2002a,b); DeLoney-Marino et al. (2003), whose genetic marker detected V. cholerae/V. mimicus. Circle (°) sizes correspond to concentrations, but note the breaks are scaled for clearer visualization, and not linearly. (×) indicates no V. cholerae found in that sample.

Figure 6

V. parahaemolyticus favors high temperatures but is relatively unconstrained by salinity. Concentrations, i.e., MPN-estimated CFU or molecular marker gene copies per 100 mL, reported in different studies are plotted against the temperature (°C) and salinity values (ppt or psu) at which they were found in bulk water samples. Circle (°) correspond to concentrations, but note the breaks are scaled for clearer visualization, and not linearly. (×) indicates no V. parahaemolyticus found in that sample.