Environmental Drivers of Vibrio cholerae Abundances in Mobile Bay, Alabama

Abstract

Vibrio cholerae is the etiological agent of the illness cholera. However, there are non-O1/non-O139 V. cholerae (NOVC) strains that generally lack the toxin gene (ctx) and colonization factors that cause cholera. These NOVC strains are autochthonous members of estuarine environments and a significant cause of seafood-borne gastroenteritis in the United States. The objective of this study was to identify environmental parameters that correlate with NOVC prevalence in oysters, water, and sediment at three ecologically diverse locations in Mobile Bay, AL, including Dog River (DR), Fowl River (FR), and Cedar Point (CP). Oyster, water, and sediment samples were collected twice a month when conditions were favorable for NOVC growth and once a month when they were not. A most probable number (MPN)/real-time PCR assay was used to determine NOVC abundances. Environmental parameters were measured during sampling to determine their relationship, if any, with NOVC at each site. NOVC abundances in oysters at DR, FR, and CP were 0.87, 0.87, and -0.13 log MPN/g, respectively. In water, the median NOVC levels at DR, FR, and CP were 1.18, -0.13, and -0.82 log MPN/mL, and in sediment, the levels were 1.48, 1.87, and -0.03 log MPN/g, respectively. Correlations of NOVC abundances in oyster, water, and sediment samples with environmental parameters were largely site specific. For example, the levels of NOVC in oysters at DR had a positive correlation with temperature but a negative correlation with dissolved oxygen (DO) and nutrient concentrations, NO₂^-, NO₃^-, dissolved inorganic nitrogen (DIN), total dissolved nitrogen (TDN), and dissolved inorganic phosphorus (DIP). At FR, however, the levels of NOVC in oysters displayed only a negative correlation with NO₂^-. When grouping NOVC abundances by temperature, the main driving factor for prevalence, additional correlations with salinity, total cell counts, dissolved organic nitrogen (DON), and dissolved organic carbon (DOC) became evident regardless of the site. IMPORTANCE NOVC can cause gastrointestinal illness in humans, which typically occurs after the consumption of raw or undercooked seafood. Incidence rates of NOVC gastroenteritis have increased during the past decade. In this study, NOVC was enumerated from oysters, sediment, and water collected at three sites in Mobile Bay, with environmental parameters measured concurrently over the course of a year, to identify potential environmental drivers of NOVC abundances. The data from this study, from an area lacking in V. cholerae research, provide a useful baseline for risk analysis of V. cholerae infections. Defining correlations between NOVC and environmental attributes at different sites and temperatures within a dynamic system such as Mobile Bay provides valuable data to better understand the occurrence and proliferation of V. cholerae in the environment.

Keywords: Mobile Bay; NOVC; V. cholerae non-O1/O139; ompW; seasonality.

FIG 1

V. cholerae abundances in oyster (A), water (B), and sediment (C) samples at Dog River (DR), Fowl River (FR), and Cedar Point (CP). The lower boundary of each box indicates the 25th percentile, the line within the box marks the median, and the upper boundary of the box indicates the 75th percentile. Whiskers above and below the box indicate the 90th and 10th percentiles.

FIG 2

V. cholerae abundances in oyster (A), water (B), and sediment (C) samples stratified by warm and cold water temperatures (defined as temperatures above and below 20°C, respectively). The boundaries of each box indicate the 25th percentile, the median, and the 75th percentile, with whiskers indicating the 10th and 90th percentiles.

FIG 3

Schematic of the interactions between V. cholerae abundances (boxes with thick dark borders) and correlating environmental parameters (boxes with arrows pointing to V. cholerae abundances) measured during this study. Negative (−) or positive (55) correlations are shown for each site (DR, FR, and CP) and sampling period (cold or warm).

FIG 4

Vibrio cholerae sampling sites at the mouth of Dog River, Fowl River, and Cedar Point near Mobile Bay, AL. (Image courtesy of the FDA Geographic Information Systems and the U.S. Census Bureau, 2020.)