Surveillance and Genomics of Toxigenic Vibrio cholerae O1 From Fish, Phytoplankton and Water in Lake Victoria, Tanzania

The occurrence of toxigenic Vibrio cholerae O1 during a non- outbreak period in Lake Victoria was studied and genetic characteristics for environmental persistence and relatedness to pandemic strains were assessed. We analyzed 360 samples of carps, phytoplankton and water collected in 2017 during dr...

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Main Authors: Yaovi M. Gildas Hounmanou, Pimlapas Leekitcharoenphon, Rene S. Hendriksen, Tamegnon V. Dougnon, Robinson H. Mdegela, John E. Olsen, Anders Dalsgaard
Format: Article
Language:English
Published: Frontiers Media S.A. 2019-04-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fmicb.2019.00901/full
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language English
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author Yaovi M. Gildas Hounmanou
Pimlapas Leekitcharoenphon
Rene S. Hendriksen
Tamegnon V. Dougnon
Robinson H. Mdegela
John E. Olsen
Anders Dalsgaard
spellingShingle Yaovi M. Gildas Hounmanou
Pimlapas Leekitcharoenphon
Rene S. Hendriksen
Tamegnon V. Dougnon
Robinson H. Mdegela
John E. Olsen
Anders Dalsgaard
Surveillance and Genomics of Toxigenic Vibrio cholerae O1 From Fish, Phytoplankton and Water in Lake Victoria, Tanzania
Frontiers in Microbiology
Vibrio cholerae
genomics
aquatic reservoirs
African Great Lakes
microbial ecology
author_facet Yaovi M. Gildas Hounmanou
Pimlapas Leekitcharoenphon
Rene S. Hendriksen
Tamegnon V. Dougnon
Robinson H. Mdegela
John E. Olsen
Anders Dalsgaard
author_sort Yaovi M. Gildas Hounmanou
title Surveillance and Genomics of Toxigenic Vibrio cholerae O1 From Fish, Phytoplankton and Water in Lake Victoria, Tanzania
title_short Surveillance and Genomics of Toxigenic Vibrio cholerae O1 From Fish, Phytoplankton and Water in Lake Victoria, Tanzania
title_full Surveillance and Genomics of Toxigenic Vibrio cholerae O1 From Fish, Phytoplankton and Water in Lake Victoria, Tanzania
title_fullStr Surveillance and Genomics of Toxigenic Vibrio cholerae O1 From Fish, Phytoplankton and Water in Lake Victoria, Tanzania
title_full_unstemmed Surveillance and Genomics of Toxigenic Vibrio cholerae O1 From Fish, Phytoplankton and Water in Lake Victoria, Tanzania
title_sort surveillance and genomics of toxigenic vibrio cholerae o1 from fish, phytoplankton and water in lake victoria, tanzania
publisher Frontiers Media S.A.
series Frontiers in Microbiology
issn 1664-302X
publishDate 2019-04-01
description The occurrence of toxigenic Vibrio cholerae O1 during a non- outbreak period in Lake Victoria was studied and genetic characteristics for environmental persistence and relatedness to pandemic strains were assessed. We analyzed 360 samples of carps, phytoplankton and water collected in 2017 during dry and rainy seasons in the Tanzanian basin of Lake Victoria. Samples were tested using PCR (ompW and ctxA) with DNA extracted from bacterial isolates and samples enriched in alkaline peptone water. Isolates were screened with polyvalent antiserum O1 followed by antimicrobial susceptibility testing. Whole genome sequencing and bioinformatics tools were employed to investigate the genomic characteristics of the isolates. More V. cholerae positive samples were recovered by PCR when DNA was obtained from enriched samples than from isolates (69.0% vs. 21.3%, p < 0.05), irrespectively of season. We identified ten V. cholerae O1 among 22 ctxA-positive isolates. Further studies are needed to serotype the remaining ctxA-positive non-O1 strains. Sequenced strains belonged to El Tor atypical biotype of V. cholerae O1 of MLST ST69 harboring the seventh pandemic gene. Major virulence genes, ctxA, ctxB, zot, ace, tcpA, hlyA, rtxA, ompU, toxR, T6SS, alsD, makA and pathogenicity islands VPI-1, VPI-2, VSP-1, and VSP-2 were found in all strains. The strains contained Vibrio polysaccharide biosynthesis enzymes, the mshA gene and two-component response regulator proteins involved in stress response and autoinducers for quorum sensing and biofilm formation. They carried the SXT integrative conjugative element with phenotypic and genotypic resistance to aminoglycoside, sulfamethoxazole, trimethoprim, phenicol, and quinolones. Strains contained a multidrug efflux pump component and were resistant to toxic compounds with copper homeostasis and cobalt-zinc-cadmium resistance proteins. The environmental strains belonged to the third wave of the seventh pandemic and most are genetically closely related to recent outbreak strains from Tanzania, Kenya, and Uganda with as low as three SNPs difference. Some strains have persisted longer in the environment and were more related to older outbreak strains in the region. V. cholerae O1 of outbreak potential seem to persist in Lake Victoria through interactions with fish and phytoplankton supported by the optimum water parameters and intrinsic genetic features enhancing survival in the aquatic environment.
topic Vibrio cholerae
genomics
aquatic reservoirs
African Great Lakes
microbial ecology
url https://www.frontiersin.org/article/10.3389/fmicb.2019.00901/full
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spelling doaj-da6747d7c56848629c24b819c5d3fee72020-11-25T01:34:39ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2019-04-011010.3389/fmicb.2019.00901446838Surveillance and Genomics of Toxigenic Vibrio cholerae O1 From Fish, Phytoplankton and Water in Lake Victoria, TanzaniaYaovi M. Gildas Hounmanou0Pimlapas Leekitcharoenphon1Rene S. Hendriksen2Tamegnon V. Dougnon3Robinson H. Mdegela4John E. Olsen5Anders Dalsgaard6Department of Veterinary and Animal Sciences, Faculty of Health and Medical Sciences, University of Copenhagen, Copenhagen, DenmarkNational Food Institute, WHO Collaborating Center for Antimicrobial Resistance in Food Borne Pathogens and Genomics and European Union Reference Laboratory for Antimicrobial Resistance, Technical University of Denmark, Kongens Lyngby, DenmarkNational Food Institute, WHO Collaborating Center for Antimicrobial Resistance in Food Borne Pathogens and Genomics and European Union Reference Laboratory for Antimicrobial Resistance, Technical University of Denmark, Kongens Lyngby, DenmarkResearch Unit in Applied Microbiology and Pharmacology of Natural Substances, Laboratory of Research in Applied Biology, Polytechnic School of Abomey-Calavi, University of Abomey-Calavi, Cotonou, BeninDepartment of Veterinary Medicine and Public Health, College of Veterinary Medicine and Biomedical Sciences, Sokoine University of Agriculture, Morogoro, TanzaniaDepartment of Veterinary and Animal Sciences, Faculty of Health and Medical Sciences, University of Copenhagen, Copenhagen, DenmarkDepartment of Veterinary and Animal Sciences, Faculty of Health and Medical Sciences, University of Copenhagen, Copenhagen, DenmarkThe occurrence of toxigenic Vibrio cholerae O1 during a non- outbreak period in Lake Victoria was studied and genetic characteristics for environmental persistence and relatedness to pandemic strains were assessed. We analyzed 360 samples of carps, phytoplankton and water collected in 2017 during dry and rainy seasons in the Tanzanian basin of Lake Victoria. Samples were tested using PCR (ompW and ctxA) with DNA extracted from bacterial isolates and samples enriched in alkaline peptone water. Isolates were screened with polyvalent antiserum O1 followed by antimicrobial susceptibility testing. Whole genome sequencing and bioinformatics tools were employed to investigate the genomic characteristics of the isolates. More V. cholerae positive samples were recovered by PCR when DNA was obtained from enriched samples than from isolates (69.0% vs. 21.3%, p < 0.05), irrespectively of season. We identified ten V. cholerae O1 among 22 ctxA-positive isolates. Further studies are needed to serotype the remaining ctxA-positive non-O1 strains. Sequenced strains belonged to El Tor atypical biotype of V. cholerae O1 of MLST ST69 harboring the seventh pandemic gene. Major virulence genes, ctxA, ctxB, zot, ace, tcpA, hlyA, rtxA, ompU, toxR, T6SS, alsD, makA and pathogenicity islands VPI-1, VPI-2, VSP-1, and VSP-2 were found in all strains. The strains contained Vibrio polysaccharide biosynthesis enzymes, the mshA gene and two-component response regulator proteins involved in stress response and autoinducers for quorum sensing and biofilm formation. They carried the SXT integrative conjugative element with phenotypic and genotypic resistance to aminoglycoside, sulfamethoxazole, trimethoprim, phenicol, and quinolones. Strains contained a multidrug efflux pump component and were resistant to toxic compounds with copper homeostasis and cobalt-zinc-cadmium resistance proteins. The environmental strains belonged to the third wave of the seventh pandemic and most are genetically closely related to recent outbreak strains from Tanzania, Kenya, and Uganda with as low as three SNPs difference. Some strains have persisted longer in the environment and were more related to older outbreak strains in the region. V. cholerae O1 of outbreak potential seem to persist in Lake Victoria through interactions with fish and phytoplankton supported by the optimum water parameters and intrinsic genetic features enhancing survival in the aquatic environment.https://www.frontiersin.org/article/10.3389/fmicb.2019.00901/fullVibrio choleraegenomicsaquatic reservoirsAfrican Great Lakesmicrobial ecology