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 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.

Saharan dust nutrients promote Vibrio bloom formation in marine surface waters

“…The potential for particle attachment is particularly salient in the case of disease-causing species like V. cholerae or V. alginolyticus, which have both been shown to be highly responsive to dust-Fe. These species are known to associate with zooplankton and marine organisms, directly influencing their survival in the environment and routes of transmission to potential hosts (3,9,46). This study, to our knowledge, is the first to demonstrate that Vibrio species, as a model of a rapidly responding opportunistic heterotroph, are highly responsive to Saharan dust-Fe and associated nutrients and indicate a role for these bacteria in processing dust-Fe in marine ecosystems.…”

“…Like other opportunistic heterotrophic bacteria, Vibrio can have disproportionately large impacts on carbon and nutrient processing because of their ability to reproduce rapidly and respond to pulses of newly available resources (2,(5)(6)(7). Characterized as "opportunitrophs," Vibrio have a broad genomic and metabolic repertoire (8), allowing them to compete in highly variable nutrient environments ranging from the open ocean to pathogenic associations with animal hosts (3,9). This genus includes many well-known pathogens of marine organisms and humans, and disease incidence has risen sharply in the last 20 y (10,11).…”

“…Common human pathogens include the causative agent of the severe diarrheal disease cholera (Vibrio cholerae), shellfish-associated gastroenteritis (Vibrio parahaemolyticus and Vibrio vulnificus), and seawater-associated wound infections (Vibrio vulnificus and Vibrio alginolyticus) (10). Studies examining the environmental drivers and distribution of Vibrio have largely focused on the role of Vibrio in disease, generally overlooking the importance of Vibrio in the biogeochemical cycling of key nutrients and trace metals (3,4). Iron (Fe) is an essential micronutrient for Vibrio growth in the environment as well as during host invasion, where it is actively sequestered by the host to prevent bacterial colonization (9).…”

“…Saharan dust | Vibrio | iron | marine biogeochemistry | microbial ecology B acteria in the Vibrio genus are globally distributed in marine environments but typically make up a minor portion of the total microbial assemblage (1, 2); however, Vibrio have been shown to bloom in response to often poorly characterized environmental factors (3,4). Like other opportunistic heterotrophic bacteria, Vibrio can have disproportionately large impacts on carbon and nutrient processing because of their ability to reproduce rapidly and respond to pulses of newly available resources (2,(5)(6)(7).…”

Demographics of lytic viral infection of coastal ocean Vibrio

“…Water temperatures, when integrated over the preceding week, showed that the latter two days belonged to warmer temperature regimes than the first day, where the minimum for the latter was 10.7°C, and the minima for the former were 14.9°C and 14.2° [ Table 3]. Increase in temperature has been shown to be the strongest predictor of increase in total Vibrio abundance, suggesting that growth rates may have been elevated on the latter two days (Oberbeckmann et al, 2012;Takemura et al, 2014). The diversity in unique Vibrio Hsp60 sequences was also higher on the latter two warmer days, when phage predation was greater, than on the first day [ Table 1].…”