LETTER
Vibrio parahaemolyticus is the leading seafood-transmitted bacterial pathogen worldwide. It causes gastroenteritis and, rarely, lethal septicemia. The estimated 45,000 annual cases of foodborne V. parahaemolyticus infections in the United States are concerning because their incidences are rising despite control measures, in part due to the impact of changing climate on pathogen abundance and distribution (1; https://www.cdc.gov/vibrio/). Although the pandemic complex of strains of sequence type 3 (ST3) (serotype O3:K6) has dominated infections worldwide (2), in the United States and Canada, the most prevalent clinical strains are of ST36 (O4:K12), which recently spread from the Pacific into the Atlantic (3–8).
Here we report that a new lineage of V. parahaemolyticus, identified as ST631, is rapidly emerging as the predominant pathogenic clade endemic to the Atlantic coast of North America (3, 4, 8). The first reported ST631 genome came from a clinical case that occurred in Louisiana in 2007 and was traced to oysters from Florida (8). In 2009, a second ST631 clinical isolate was reported in Prince Edward Island, Canada (O11:KUT) (4). From 2010 to 2015, the incidence of infections by strains of ST631 has increased, with 35 confirmed cases reported in four Atlantic coastal U.S. states (Table 1), where they are second only to ST36 strains in prevalence. Due to the self-limiting nature of infections and underreporting (9), ST631 infections may be more widespread.
TABLE 1.
Isolate | SRA or GenBank accession no.a | State of isolationb | Trace-back locationb | Yr of isolation | Reporting countryc | Sourced | Geographic locatione |
---|---|---|---|---|---|---|---|
VP2007-095 | SRR869104 | LA | FL | 2007 | USA | C | FL |
09-4436 | LRAJ01000000 | PEI | PEI | 2009 | Canada | C | PEI |
S487-4 | LFZE01000000 | NA | Canada | 2013 | Canada | E | PEI |
MAVP-A | SRR4032168 | MA | NA | 2010 | USA | C | |
MAVP-E | SRR1952988 | MA | MA | 2010 | USA | C | GOM |
MAVP-P | SRR4032175 | MA | NA | 2010 | USA | C | |
MAVP-T | SRR4032176 | MA | NA | 2010 | USA | C | |
MAVP-L | SRR4032169 | MA | MA | 2011 | USA | C | GOM |
MAVP-Q | SRR4035056 | MA | MA | 2011 | USA | C | GOM |
MAVP-4 | SRR4032177 | MA | NA | 2013 | USA | C | |
MAVP-30 | SRR4032178 | MA | NA | 2013 | USA | C | |
MAVP-39 | SRR4032179 | MA | NA | 2013 | USA | C | |
MAVP-56 | SRR4032180 | MA | PEI | 2013 | USA | C | PEI |
MAVP-74 | SRR4032181 | MA | CT or PEI | 2014 | USA | C | LIS or PEI |
MAVP-75 | SRR4032182 | MA | CT or MA | 2014 | USA | C | GOM or LIS |
MAVP-78 | SRR4032170 | MA | MA | 2014 | USA | C | GOM |
MAVP-90 | SRR4032171 | MA | CT | 2015 | USA | C | LIS |
MAVP-94 | SRR4032172 | MA | MA | 2015 | USA | C | GOM |
MAVP-109 | SRR4032173 | MA | MA | 2015 | USA | C | GOM |
MAVP-112 | SRR4032174 | MA | MA | 2015 | USA | C | GOM |
VP1 | SRR4032354 | MD | VA | 2012 | USA | C | MAC |
VP8 | SRR4032362 | MD | NA | 2012 | USA | C | |
VP9 | SRR4032363 | MD | NJ | 2012 | USA | C | MAC |
VP31 | SRR4032355 | MD | NJ | 2013 | USA | C | MAC |
VP35 | SRR4032356 | MD | NA | 2013 | USA | C | |
VP41 | SRR4032357 | MD | NA | 2013 | USA | C | |
VP44 | SRR4032358 | MD | NA | 2013 | USA | C | |
VP45 | SRR4032359 | MD | CT or VA | 2013 | USA | C | LIS or MAC |
VP47 | SRR4032360 | MD | NA | 2013 | USA | C | |
VP55 | SRR4032361 | MD | NA | 2014 | USA | C | |
PNUSAV000012 | SRR4016797 | MD | CT, MA, or ME | 2015 | USA | C | GOM or LIS |
PNUSAV000015 | SRR4016801 | MD | CT, MA, NY, PEI, or VA | 2015 | USA | C | GOM, LIS, MAC, or PEI |
PNUSAV00021 | SRR4018053 | MD | NA | 2015 | USA | C | |
CTVP27C | SRR4090622 | CT | CT or VA | 2013 | USA | C | LIS or MAC |
CTVP31C | SRR4090623 | CT | NA | 2013 | USA | C | |
CTVP34C | SRR4090624 | CT | NA | 2013 | USA | C | |
MEVP-12 | SRR4090625 | ME | NA | 2015 | USA | C | |
MEVP-14 | SRR4090626 | ME | NA | 2015 | USA | C |
Massachusetts, Connecticut, and Maine isolates were sequenced using the Illumina HiSeq2500 sequencer at the Hubbard Center for Genomic Studies at the University of New Hampshire, whereas Maryland isolates were sequenced using the Illumina MiSeq sequencer at the Center for Food Safety and Applied Nutrition, Food and Drug Administration, Maryland, or at the Department of Health and Hygiene, Maryland.
Where available, the U.S. state or Canadian location of isolation and infection is identified. For multisource traces, all possible sources are listed. CT, Connecticut; FL, Florida; LA, Louisiana; MA, Massachusetts; ME, Maine; NA, information was not available or was not determined; NJ, New Jersey; NY, New York; PEI, Prince Edward Island; VA, Virginia.
The country which reported the isolate.
C, clinical isolate; E, environmental isolate (specifically, from an oyster).
The geographic locations of the sources corresponding to those identified in Fig. 1A. These include Florida (FL), the Gulf of Maine (GOM), Long Island Sound (LIS), the Mid-Atlantic Coast (MAC), and Prince Edward Island (PEI).
Genome comparisons were used to understand the potential relationships of ST631 strains, which share no recent ancestry with and differ substantially from ST36 and ST3 strains (>3,600 out of 3,909 shared genes contained variation). ST631 has a virulence gene profile similar to that of ST36 in that it harbors tdh, trh, and a type 3 secretion system (T3SS2) and is urease positive. We applied a core genome multilocus typing (cgMLST) scheme to draft genomes of 37 clinical isolates and 1 environmental isolate (Table 1) representing the geographic and time spans of infections. This analysis identified 132 single nucleotide polymorphisms (SNPs) in the population and confirmed that clinical ST631 isolates are clonal, with limited diversification (Fig. 1). Within the ST631 population, 97% of the core genes are identical, whereas less than 8% of the core genes are identical between ST631, ST36, and ST3 strains. Both maximum-likelihood phylogeny and minimum spanning tree analysis indicated a mixed population (Fig. 1A and B). Most isolates grouped within one clonal complex, with only a few divergent isolates (Fig. 1B). This population structure suggests that this pathogenic lineage recently evolved and that its distribution may have expanded along the North American Atlantic Coast (10).
The fact that an increasing number of cases tracing to sources in the northwestern Atlantic suggests that ST631 poses a mounting public health threat and calls for surveillance of this lineage to reduce illnesses. That its emergence coincided with warming ocean trends in some areas of the northwestern Atlantic (2) and invasion by a nonresident pathogen indicates that a changing climate may be driving pathogen dynamics (1, 2, 3, 7). However, this does not eliminate the potential of anthropogenic influences on the dissemination of ST631 strains, whose continued population expansion may increase human health risk beyond North America.
Accession number(s).
Sequences were deposited in the Sequence Read Archive under accession numbers SRR1952988, SRR4016797, SRR4016801, SRR4018053, SRR4032168 to SRR4032182, SRR4032354 to SRR4032363, SRR4035056, and SRR4090622 to SRR4090626.
ACKNOWLEDGMENTS
Feng Xu and Cheryl A. Whistler declare a potential conflict of interest in the form of a pending patent application (U.S. patent application 62/128,764).
Partial funding for this work was provided by the USDA National Institute of Food and Agriculture (Hatch projects NH00574, NH00609 [accession number 233555], and NH00625 [accession number 1004199]). Additional funding was provided by the National Oceanic and Atmospheric Administration College Sea Grant program and grants R/CE-137, R/SSS-2, and R/HCE-3. Support was also provided through the National Institutes of Health (1R03AI081102-01), the National Science Foundation (EPSCoR IIA-1330641), and the National Science Foundation (DBI 1229361 NSF MRI). N.G.-E. was funded through the FDA Foods Science and Research Intramural Program.
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