Cooper, Vaughn S.

DeRosia-Banick, Kristin

Ferguson, Jana

Gonzalez-Escalona, Narjol

Haendiges, Julie

Hickey, Eric

Hickey, John Michael

Jones, Stephen H.

Mank, Laurn

Matluk, Nicholas

Moore, Michael

Myers, Robert A.

Robbins, Amy

Schillaci, Christopher

Sebra, Robert P.

Stiles, Tracy

Whistler, Cheryl A.

Xu, Feng

English

PubMed

UNH Scholars' Repository

University of New Hampshire University of New Hampshire Scholars' Repository New Hampshire EPSCoR Research Institutes, Centers and Programs 1-25-2017 Sequence Type 631 Vibrio parahaemolyticus, an Emerging Foodborne Pathogen in North America Feng Xu University of New Hampshire, Durham Narjol Gonzalez-Escalona College Park Julie Haendiges Department of Health and Mental Hygiene Robert A. Myers Department of Health and Mental Hygiene Jana Ferguson Massachusetts Department of Public Health See next page for additional authors Follow this and additional works at: https://scholars.unh.edu/nh_epscor Comments This is an Open Access article published by American Society for Microbiology in Journal of Clinical Microbiology in 2017, available online: https://dx.doi.org/10.1128/JCM.02162-16 Recommended Citation Xu, F., Gonzalez-Escalona, N., Haendiges, J., Myers, R.A., Ferguson, J., Stiles, T., ... & Whistler, C.A. (2017) Sequence Type 631 Vibrio parahaemolyticus, an Emerging Foodborne Pathogen in North America, Journal of Clinical Microbiology, 55(2), 645–648. doi:10.1128/jcm.02162-16. This Article is brought to you for free and open access by the Research Institutes, Centers and Programs at University of New Hampshire Scholars' Repository. It has been accepted for inclusion in New Hampshire EPSCoR by an authorized administrator of University of New Hampshire Scholars' Repository. For more information, please contact Scholarly.Communication@unh.edu. Authors Feng Xu, Narjol Gonzalez-Escalona, Julie Haendiges, Robert A. Myers, Jana Ferguson, Tracy Stiles, Eric Hickey, Michael Moore, John Michael Hickey, Christopher Schillaci, Laurn Mank, Kristin DeRosia-Banick, Nicholas Matluk, Amy Robbins, Robert P. Sebra, Vaughn S. Cooper, Stephen H. Jones, and Cheryl A. Whistler This article is available at University of New Hampshire Scholars' Repository: https://scholars.unh.edu/nh_epscor/164 Sequence Type 631 Vibrioparahaemolyticus, an EmergingFoodborne Pathogen in North AmericaFeng Xu,a,b,c Narjol Gonzalez-Escalona,d Julie Haendiges,e Robert A. Myers,eJana Ferguson,f Tracy Stiles,f Eric Hickey,f Michael Moore,f John Michael Hickey,gChristopher Schillaci,g Laurn Mank,h Kristin DeRosia-Banick,i Nicholas Matluk,jAmy Robbins,j Robert P. Sebra,k Vaughn S. Cooper,a,b,l Stephen H. Jones,a,mCheryl A. Whistlera,bNortheast Center for Vibrio Disease and Ecology, University of New Hampshire, Durham, New Hampshire,USAa; Department of Molecular, Cellular, and Biomedical Sciences, University of New Hampshire,Durham, New Hampshire, USAb; Genetics Graduate Program, University of New Hampshire, Durham, NewHampshire, USAc; Center for Food Safety and Applied Nutrition, Food and Drug Administration, CollegePark, Maryland, USAd; Department of Health and Mental Hygiene, Baltimore, Maryland, USAe;Massachusetts Department of Public Health, Boston, Massachusetts, USAf; Massachusetts Division ofMarine Fisheries, New Bedford, Massachusetts, USAg; Department of Public Health Laboratory, Rocky Hill,Connecticut, USAh; Department of Agriculture, Bureau of Aquaculture, State of Connecticut, Milford,Connecticut, USAi; Department of Health and Human Services, Augusta, Maine, USAj; Icahn Institute andDepartment of Genetics & Genomic Sciences, Icahn School of Medicine at Mount Sinai, New York, NewYork, USAk; Microbiology and Molecular Genetics, University of Pittsburgh School of Medicine, Pittsburgh,Pennsylvania, USAl; Department of Natural Resources and the Environment, University of NewHampshire, Durham, New Hampshire, USAmKEYWORDS Vibrio parahaemolyticus, core genome multilocus sequence typeanalysis, emerging pathogen, genomics, molecular epidemiologyVibrio parahaemolyticus is the leading seafood-transmitted bacterial pathogenworldwide. It causes gastroenteritis and, rarely, lethal septicemia. The estimated45,000 annual cases of foodborne V. parahaemolyticus infections in the United Statesare concerning because their incidences are rising despite control measures, in part dueto the impact of changing climate on pathogen abundance and distribution (1;https://www.cdc.gov/vibrio/). Although the pandemic complex of strains of sequencetype 3 (ST3) (serotype O3:K6) has dominated infections worldwide (2), in the UnitedStates and Canada, the most prevalent clinical strains are of ST36 (O4:K12), whichrecently spread from the Pacific into the Atlantic (3–8).Here we report that a new lineage of V. parahaemolyticus, identified as ST631, israpidly emerging as the predominant pathogenic clade endemic to the Atlanticcoast of North America (3, 4, 8). The first reported ST631 genome came from aclinical case that occurred in Louisiana in 2007 and was traced to oysters fromFlorida (8). In 2009, a second ST631 clinical isolate was reported in Prince EdwardIsland, Canada (O11:KUT) (4). From 2010 to 2015, the incidence of infections bystrains of ST631 has increased, with 35 confirmed cases reported in four Atlanticcoastal U.S. states (Table 1), where they are second only to ST36 strains in preva-lence. Due to the self-limiting nature of infections and underreporting (9), ST631infections may be more widespread.Genome comparisons were used to understand the potential relationships of ST631strains, which share no recent ancestry with and differ substantially from ST36 and ST3strains (3,600 out of 3,909 shared genes contained variation). ST631 has a virulencegene profile similar to that of ST36 in that it harbors tdh, trh, and a type 3 secretionsystem (T3SS2) and is urease positive. We applied a core genome multilocus typingAccepted manuscript posted online 14December 2016Citation Xu F, Gonzalez-Escalona N, HaendigesJ, Myers RA, Ferguson J, Stiles T, Hickey E,Moore M, Hickey JM, Schillaci C, Mank L,Derosia-Banick K, Matluk N, Robbins A, SebraRP, Cooper VS, Jones SH, Whistler CA. 2017.Sequence type 631 Vibrio parahaemolyticus, anemerging foodborne pathogen in NorthAmerica. J Clin Microbiol 55:645– 648. https://doi.org/10.1128/JCM.02162-16.Editor Karen C. Carroll, The Johns HopkinsUniversity School of MedicineCopyright © 2017 Xu et al. This is an open-access article distributed under the terms ofthe Creative Commons Attribution 4.0International license.Address correspondence to Narjol Gonzalez-Escalona, narjol.gonzalez-escalona@fda.hhs.gov.LETTER TO THE EDITORcrossmFebruary 2017 Volume 55 Issue 2 jcm.asm.org 645Journal of Clinical MicrobiologyDownloaded from https://journals.asm.org/journal/jcm on 24 March 2023 by 71.232.151.1.(cgMLST) scheme to draft genomes of 37 clinical isolates and 1 environmental isolate (Table1) representing the geographic and time spans of infections. This analysis identified 132single nucleotide polymorphisms (SNPs) in the population and confirmed that clinicalST631 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 identicalbetween ST631, ST36, and ST3 strains. Both maximum-likelihood phylogeny and minimumspanning tree analysis indicated a mixed population (Fig. 1A and B). Most isolates groupedwithin one clonal complex, with only a few divergent isolates (Fig. 1B). This populationstructure suggests that this pathogenic lineage recently evolved and that its distributionmay have expanded along the North American Atlantic Coast (10).The fact that an increasing number of cases tracing to sources in the northwesternAtlantic suggests that ST631 poses a mounting public health threat and calls forsurveillance of this lineage to reduce illnesses. That its emergence coincided withTABLE 1 ST631 isolates with relevant informationIsolateSRA or GenBankaccession no.aState ofisolationb Trace-back locationbYr ofisolationReportingcountryc Sourced Geographic locationeVP2007-095 SRR869104 LA FL 2007 USA C FL09-4436 LRAJ01000000 PEI PEI 2009 Canada C PEIS487-4 LFZE01000000 NA Canada 2013 Canada E PEIMAVP-A SRR4032168 MA NA 2010 USA CMAVP-E SRR1952988 MA MA 2010 USA C GOMMAVP-P SRR4032175 MA NA 2010 USA CMAVP-T SRR4032176 MA NA 2010 USA CMAVP-L SRR4032169 MA MA 2011 USA C GOMMAVP-Q SRR4035056 MA MA 2011 USA C GOMMAVP-4 SRR4032177 MA NA 2013 USA CMAVP-30 SRR4032178 MA NA 2013 USA CMAVP-39 SRR4032179 MA NA 2013 USA CMAVP-56 SRR4032180 MA PEI 2013 USA C PEIMAVP-74 SRR4032181 MA CT or PEI 2014 USA C LIS or PEIMAVP-75 SRR4032182 MA CT or MA 2014 USA C GOM or LISMAVP-78 SRR4032170 MA MA 2014 USA C GOMMAVP-90 SRR4032171 MA CT 2015 USA C LISMAVP-94 SRR4032172 MA MA 2015 USA C GOMMAVP-109 SRR4032173 MA MA 2015 USA C GOMMAVP-112 SRR4032174 MA MA 2015 USA C GOMVP1 SRR4032354 MD VA 2012 USA C MACVP8 SRR4032362 MD NA 2012 USA CVP9 SRR4032363 MD NJ 2012 USA C MACVP31 SRR4032355 MD NJ 2013 USA C MACVP35 SRR4032356 MD NA 2013 USA CVP41 SRR4032357 MD NA 2013 USA CVP44 SRR4032358 MD NA 2013 USA CVP45 SRR4032359 MD CT or VA 2013 USA C LIS or MACVP47 SRR4032360 MD NA 2013 USA CVP55 SRR4032361 MD NA 2014 USA CPNUSAV000012 SRR4016797 MD CT, MA, or ME 2015 USA C GOM or LISPNUSAV000015 SRR4016801 MD CT, MA, NY, PEI, or VA 2015 USA C GOM, LIS, MAC, or PEIPNUSAV00021 SRR4018053 MD NA 2015 USA CCTVP27C SRR4090622 CT CT or VA 2013 USA C LIS or MACCTVP31C SRR4090623 CT NA 2013 USA CCTVP34C SRR4090624 CT NA 2013 USA CMEVP-12 SRR4090625 ME NA 2015 USA CMEVP-14 SRR4090626 ME NA 2015 USA CaMassachusetts, Connecticut, and Maine isolates were sequenced using the Illumina HiSeq2500 sequencer at the Hubbard Center for Genomic Studies at theUniversity 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.bWhere 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 EdwardIsland; VA, Virginia.cThe country which reported the isolate.dC, clinical isolate; E, environmental isolate (specifically, from an oyster).eThe 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).Letter to the Editor Journal of Clinical MicrobiologyFebruary 2017 Volume 55 Issue 2 jcm.asm.org 646Downloaded from https://journals.asm.org/journal/jcm on 24 March 2023 by 71.232.151.1.warming ocean trends in some areas of the northwestern Atlantic (2) and invasion bya nonresident pathogen indicates that a changing climate may be driving pathogendynamics (1, 2, 3, 7). However, this does not eliminate the potential of anthropogenicinfluences on the dissemination of ST631 strains, whose continued population expan-sion may increase human health risk beyond North America.Accession number(s). Sequences were deposited in the Sequence Read Archive underaccession numbers SRR1952988, SRR4016797, SRR4016801, SRR4018053, SRR4032168to SRR4032182, SRR4032354 to SRR4032363, SRR4035056, and SRR4090622 toSRR4090626.ACKNOWLEDGMENTSFeng Xu and Cheryl A. Whistler declare a potential conflict of interest in the form ofa pending patent application (U.S. patent application 62/128,764).Partial funding for this work was provided by the USDA National Institute of Foodand Agriculture (Hatch projects NH00574, NH00609 [accession number 233555], andNH00625 [accession number 1004199]). Additional funding was provided by the Na-tional Oceanic and Atmospheric Administration College Sea Grant program and grantsR/CE-137, R/SSS-2, and R/HCE-3. Support was also provided through the NationalInstitutes of Health (1R03AI081102-01), the National Science Foundation (EPSCoR IIA-1330641), and the National Science Foundation (DBI 1229361 NSF MRI). N.G.-E. wasfunded through the FDA Foods Science and Research Intramural Program.REFERENCES1. Baker-Austin C, Trinanes JA, Taylor NG, Hartnell R, Siitonen A, Martinez-Urtaza J. 2013. Emerging Vibrio risk at high latitudes in response toocean warming. Nat Clim Change 3:73–77.2. Vezzulli L, Grande C, Reid P, Helaouet P, Edwards M, Hofle MG, BrettardI, Colwell RR, Pruzzo C. 2016. Climate influence on Vibrio and associatedhuman diseases during the past half-century in the coastal North Atlan-tic. Proc Natl Acad Sci U S A 13:E5062–E5071. https://doi.org/10.1073/pnas.1609157113.3. Xu F, Ilyas S, Hall JA, Jones SH, Cooper VS, Whistler CA. 2015. Geneticcharacterization of clinical and environmental Vibrio parahaemolyticusFIG 1 Phylogenetic relationships among ST631 isolates traced to the northwestern Atlantic (2007 to 2015). (A) A maximum-likelihood tree constructed with thecore genome SNPs identified from cluster analysis (described below) of 35 newly sequenced clinical isolates reported in Massachusetts, Maryland, Maine, andConnecticut and 3 isolates whose draft genomes were publicly available in the NCBI database (strains 09-4436, S487-4, and VP2007-95) (Table 1) demonstratesthe highly clonal nature of pathogenic ST631 isolates, which are colored by year and marked by geographic distribution. The scale bar represents the averagenumber of nucleotide substitutions per site, and branches with greater than 60% bootstrap support are labeled. (B) A minimum spanning tree analysis reflectingthe relationships among ST631 isolates based on core gene SNPs differences further demonstrates the clonal population structure. The numbers above theconnected lines (not to scale) represent SNP differences. The isolates are colored by year of isolation using the same color scheme as in panel A. Cluster analysisof ST631 was performed using a custom cgMLST analysis using Ridom SeqSphere software v3.2.1 (Ridom GmbH, Münster, Germany). Briefly, the cgMLSTsoftware first defines a cgMLST scheme using the cgMLST target definer tool with default settings. MAVP-Q was used as the reference genome (4,568 genes).Then, five other V. parahaemolyticus genomes (strains BB22OP, CDC_K4557, FDA_R31, RIMD 2210633, and UCM-V493) were used for comparison with thereference genome to establish the core and accessory genome genes. Genes that are repeated in more than one copy in any of the six genomes were removed fromthe analysis. Subsequently, a task template that contains both core and accessory genes was created. Each individual gene locus from MAVP-Q was assigned allelenumber 1. Then each individual ST631 V. parahaemolyticus genome assembly was queried against the task template, during which any locus that differed from thereference genome or any other queried genome was assigned a new allele number. For the cgMLST, a gene-by-gene analysis of all core genes (excluding accessorygenes) was performed and SNPs were identified within different alleles to establish genetic distance calculations. PEI, Prince Edward Island; FL, Florida.Letter to the Editor Journal of Clinical MicrobiologyFebruary 2017 Volume 55 Issue 2 jcm.asm.org 647Downloaded from https://journals.asm.org/journal/jcm on 24 March 2023 by 71.232.151.1.from the Northeast U.S.A. reveals emerging resident and non-indigenous pathogen lineages. Front Microbiol 6:272. https://doi.org/10.3389/fmicb.2015.00272.4. Banerjee SK, Kearney AK, Nadon CA, Peterson C-L, Tyler K, Bakouche L,Clark CG, Hoang L, Gilmour MW, Farber JM. 2014. Phenotypic andgenotypic characterization of Canadian clinical isolates of Vibrio parah-aemolyticus collected from 2000 to 2009. J Clin Microbiol 52:1081–1088.https://doi.org/10.1128/JCM.03047-13.5. Turner JW, Paranjpye RN, Landis ED, Biryukov SV, González-Escalona N,Nilsson WB, Strom MS. 2013. Population structure of clinical and envi-ronmental Vibrio parahaemolyticus from the Pacific Northwest coast ofthe United States. PLoS One 8:e55726. https://doi.org/10.1371/journal.pone.0055726.6. García K, Bastías R, Higuera G, Torres R, Mellado A, Uribe P, Espejo RT.2013. Rise and fall of pandemic Vibrio parahaemolyticus serotype O3:K6in southern Chile. Environ Microbiol 15:527–534. https://doi.org/10.1111/j.1462-2920.2012.02883.x.7. Martinez-Urtaza J, Baker-Austin C, Jones JL, Newton AE, Gonzalez-AvilesGD, DePaola A. 2013. Spread of Pacific Northwest Vibrio parahaemolyti-cus strain. N Engl J Med 369:1573–1574. https://doi.org/10.1056/NEJMc1305535.8. Haendiges J, Timme R, Allard MW, Myers RA, Brown EW, Gonzalez-Escalona N. 2015. Characterization of Vibrio parahaemolyticus clinicalstrains from Maryland (2012–2013) and comparisons to locally andglobally diverse V. parahaemolyticus strains by whole-genome sequenceanalysis. Front Microbiol 6:125. https://doi.org/10.3389/fmicb.2015.00125.9. Scallan E, Hoekstra RM, Angulo FJ, Tauxe RV, Widdowson M-A, Roy SL,Jones JL, Griffin PM. 2011. Foodborne illnesses acquired in the UnitedStates—major pathogens. Emerg Infect Dis 17:7–15. https://doi.org/10.3201/eid1701.P11101.10. Jonsson BF, Watson JR. 2016. The timescale of global surface oceanconnectivity. Nat Commun 7:11239. https://doi.org/10.1038/ncomms11239.Letter to the Editor Journal of Clinical MicrobiologyFebruary 2017 Volume 55 Issue 2 jcm.asm.org 648Downloaded from https://journals.asm.org/journal/jcm on 24 March 2023 by 71.232.151.1.

Sequence Type 631 Vibrio parahaemolyticus, an Emerging Foodborne Pathogen in North America

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Sequence Type 631 Vibrio parahaemolyticus, an Emerging Foodborne Pathogen in North America

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