ABSTRACT
Vibrio species are indigenous to the marine and estuarine environments around the world and are the leading cause of water- and seafood-borne illnesses due to conditions favoring the transmission and growth of the species. Horizontal gene transfer, recombination, and mutation enable Vibrio spp. to adapt rapidly to environmental challenges from biotic and abiotic parameters, including temperature, salinity, and nutrient status of the coastal waters. This surveillance study provides evidence of Vibrio cholerae emerging in the temperate estuaries of Canada, thereby redefining the diversity and dynamics of its coastal Vibrio population. The presence of the pathogenic context in Vibrio parahaemolyticus was also detected with an increasing trend during the study period.
IMPORTANCE Proliferation and abundance of the harmful biotypes of Vibrio spp. in the estuaries of Canada indicate the possibility of producing contaminated seafood for human consumption. The findings of this surveillance study may lead to awareness which may help efforts to reduce the occurrence of illnesses or outbreaks caused by Vibrio spp. in seafood.
INTRODUCTION
Vibrios are ubiquitous in marine and estuarine environments around the world, with more than 100 species identified, among which the most clinically significant species are Vibrio cholerae, Vibrio parahaemolyticus, and Vibrio vulnificus (1, 2). Cholera, caused by V. cholerae, is known to be linked to specific seasons and biogeographical zones based on warmer temperatures and ecology; it is an ancient disease which has killed millions of people from the warm tropical to the cold temperate regions of the world (1–4). This disease had disappeared from most of the developed world by the end of the 20th century, but it remained endemic in many tropical regions (4). In recent years, cholera has been detected in and reported from many developed countries in the temperate regions of the world (5–9). Among the prominent halophilic Vibrio spp., V. parahaemolyticus is the leading cause of seafood-associated illness around the world and, in North America, it prevails with extreme diversity (6, 8). Since emerging in the Far East (Japan) in the 1950s, this species has caused many seafood-borne outbreaks in the world by the identified pandemic strain and its serovariants (3, 10). The majority of the clinical isolates carry one or both of two hemolysin genes, encoding thermostable direct hemolysin (TDH) (11) and TDH-related hemolysin (TRH) (12). V. vulnificus is a highly lethal and opportunistic pathogen known to cause most seafood-related mortality in the United States (13). This surveillance study highlights two major trends of concern to human health in Canada as well as other temperate regions of the world, (i) the emergence of V. cholerae and (ii) the increase in detection of potentially pathogenic V. parahaemolyticus strains, isolated from molluscan shellfish harvested in Canada during the warmer months of 2006 to 2016.
RESULTS AND DISCUSSION
During the 11-year period (2006 to 2016), five identified Vibrio spp., comprising halophilic (V. parahaemolyticus, V. vulnificus, V. fluvialis, and V. alginolyticus) as well as nonhalophilic V. cholerae strains, were isolated with various frequencies of detection (Fd). In addition, unidentified Vibrio spp. of marine origin were detected in large numbers and were included in the analysis (Fig. 1). As seen in Fig. 1, the Fd for V. parahaemolyticus increased from 41% (2006 to 2009, P1) to 69% (2010 to 2013, P2) and 63% (2014 to 2016, P3) for the east coast molluscan samples, while the values were 57% (P1) and 62% (P2) for the west coast samples during the defined periods. The values for V. alginolyticus remained more or less stable but high (83% to 97%). The tropical species V. cholerae emerged with an increased Fd in the later periods. On the east coast, the Fd for V. cholerae jumped to 20% (P3) from 1% (P1 and P2), while on the west coast, the value increased from 1% (P1) to 5% (P2). The Fd values for V. vulnificus were more or less stable on either coast, with 20% for the east (P1, P2, and P3), and 11% (P1) to 9% (P2) for the west. Unidentified Vibrio spp. were detected in the range of 13% (P1, east) to 27% (P2, west). Data for the west coast molluscs during P3 are not included, as samplings were interrupted, and the few available data will have to be repeated and merged with ongoing data. This study revealed the presence of a trend in the composition of the Vibrio community in Canadian coastal waters, which may be driven by climate change. The observed composition in interspecies diversity of the genus Vibrio with increasing abundance of V. cholerae strains, which are endemic in the tropical regions of the world, supports the notion that V. cholerae strains are emerging in the Canadian waters. Follow-up studies are required to investigate the influence of environmental factors on the Vibrio community composition associated with the specific harvest sites. Historically, cholera is known to have reappeared in areas from where it had been absent for many years, and it has also emerged in newer communities, resulting in an expanded area of endemicity (4).
Normalized (percent) proportions of the individual Vibrio species detected during the study period, divided into segments/periods (P) to observe the trend and dynamics. Vp, V. parahaemolyticus; Va, V. alginolyticus; Vv, V. vulnificus; Vc, V. cholerae; Vf, V. fluvialis; Vspp, Vibrio species; P1, 2006 to 2009; P2, 2010 to 2013; P3, 2014 to 2016. The arrows point to the significant increases in Vc prevalence.
Coinciding with the increasing emergence of V. cholerae isolates, there was also an increase in the number of molluscan V. parahaemolyticus isolates testing positive for virulence markers by PCR (Fig. 2). Coincidentally, the rise in frequency of potentially pathogenic V. parahaemolyticus strains was significant on the east coast (14.6% in P1 to 27.9% in P2), as opposed to the trend on the west coast (6.6% in P1 to 9.4% in P2). During the same study period, V. parahaemolyticus isolates increasingly tested positive for the pathogenic hemolysin genes (tdh and trh) associated with gastroenteritis in human beings in Canada. Seasonality is attributed to V. parahaemolyticus infections, as this organism causes most of the illnesses in the warmer months of the year in temperate regions (3, 14). The dynamics of V. parahaemolyticus infection and the diversity of the causative strains testify to the existence of many variants of this species as a result of its genome plasticity and adaptability to climate changes (1, 3, 4). Hence, the impact of the warming trend on the proliferation and abundance of disease-causing hemolysin genes in molluscan V. parahaemolyticus strains indicates a correlation which requires further investigation.
Frequency of harvested molluscan shellfish samples testing positive for potentially pathogenic V. parahaemolyticus (pVp). The data were averaged over successive 4-year periods and normalized (percent), as shown, to observe the trend.
Both findings indicate that pursuing and studying the Canadian Vibrio community over a long period of time will be useful for ecosystem assessment. This scientific information may help develop strategies to reduce the occurrence of illnesses or outbreaks caused by Vibrio spp. in seafood and to assess the adverse effects of climate change in Canadian estuaries.
MATERIALS AND METHODS
Bivalve molluscs (clams, mussels, and oysters), which are filter feeders of planktons and marine pollutants, were sampled from the coastal waters of British Columbia (Canadian Pacific coast) and the Gaspé Peninsula in Québec, as well as the Digby and Yarmouth counties in Nova Scotia (Canadian Atlantic coast), for the presence of Vibrio species, particularly V. parahaemolyticus, V. vulnificus, V. cholerae, V. fluvialis, and V. alginolyticus, from May to October of each year from 2006 to 2016. Biochemical and molecular assays, including PCR, targeting the virulent hemolysin genes of V. parahaemolyticus were used to identify and characterize the isolates (15, 16). The study period was divided into three parts, P1 (2006 to 2009), P2 (2010 to 2013), and P3 (2014 to 2016), spanning 3 to 4 years and normalized (percent) per year to express the percent prevalence (frequency of detection [Fd]) of each species. Data from the east (Atlantic) and the west (Pacific) coasts of Canada were analyzed separately.
ACKNOWLEDGMENTS
This study was supported by funding from the Government of Canada (GoC) to S.K.B. of Health Canada for surveillance research related to seafood safety.
We thank all personnel in the facility for preparation of media of our bureau, as well as the students who helped during the study period. We are thankful to Brent Dixon and Januana Teixeira of our research division for peer reviewing the manuscript and providing helpful comments.
FOOTNOTES
- Received 4 January 2018.
- Accepted 2 May 2018.
- Accepted manuscript posted online 7 May 2018.
- Address correspondence to Swapan K. Banerjee, swapan.banerjee{at}canada.ca.
Citation Banerjee SK, Rutley R, Bussey J. 2018. Diversity and dynamics of the Canadian coastal Vibrio community: an emerging trend detected in the temperate regions. J Bacteriol 200:e00787-17. https://doi.org/10.1128/JB.00787-17.
REFERENCES
- © Crown copyright 2018.
The government of Australia, Canada, or the UK (“the Crown”) owns the copyright interests of authors who are government employees. The Crown Copyright is not transferable.
