Microbiomes of pathogenic Vibrio species reveal environmental and planktonic associations

Background Many species of coastal Vibrio spp. bacteria can infect humans, representing an emerging health threat linked to increasing seawater temperatures. Vibrio interactions with the planktonic community impact coastal ecology and human infection potential. In particular, interactions with eukaryotic and photosynthetic organism may provide attachment substrate and critical nutrients (e.g. chitin, phytoplankton exudates) that facilitate the persistence, diversification, and spread of pathogenic Vibrio spp. Vibrio interactions with these organisms in an environmental context are, however, poorly understood.Results We quantified pathogenic Vibrio species, including V. cholerae, V. parahaemolyticus, and V. vulnificus, and two virulence-associated genes for one year at five coastal sites in Southern California and used metabarcoding to profile associated prokaryotic and eukaryotic communities, including vibrio-specific communities. These Vibrio spp. reached high abundances, particularly during Summer months, and inhabited distinct species-specific environmental niches driven by temperature and salinity. Associated bacterial and eukaryotic taxa identified at fine-scale taxonomic resolution revealed genus and species-level relationships. For example, common Thalassiosira genera diatoms capable of exuding chitin were positively associated with V. cholerae and V. vulnificus in a species-specific manner, while the most abundant eukaryotic genus, the diatom Chaetoceros, was positively associated with V. parahaemolyticus. Associations were often linked to shared environmental preferences, and several copepod genera were linked to low-salinity environmental conditions and abundant V. cholerae and V. vulnificus.Conclusions This study clarifies ecological relationships between pathogenic Vibrio spp. and the planktonic community, elucidating new functionally relevant associations, establishing a workflow for examining environmental pathogen microbiomes, and highlighting prospective model systems for future mechanistic studies.

[1]  D. Raftos,et al.  Simulated Marine Heat Wave Alters Abundance and Structure of Vibrio Populations Associated with the Pacific Oyster Resulting in a Mass Mortality Event , 2018, Microbial Ecology.

[2]  Francesco Asnicar,et al.  QIIME 2: Reproducible, interactive, scalable, and extensible microbiome data science , 2018 .

[3]  M. Blokesch,et al.  Eco-evolutionary Dynamics Linked to Horizontal Gene Transfer in Vibrios. , 2018, Annual review of microbiology.

[4]  E. Armbrust,et al.  Comparative Genomic Analysis of Vibrio diabolicus and Six Taxonomic Synonyms: A First Look at the Distribution and Diversity of the Expanded Species , 2018, Front. Microbiol..

[5]  M. Waldor,et al.  Vibrio spp. infections , 2018, Nature Reviews Disease Primers.

[6]  R. Noble,et al.  Vibrio Ecology in the Neuse River Estuary, North Carolina, Characterized by Next-Generation Amplicon Sequencing of the Gene Encoding Heat Shock Protein 60 (hsp60) , 2018, Applied and Environmental Microbiology.

[7]  M. Hildebrand,et al.  Understanding Diatom Cell Wall Silicification—Moving Forward , 2018, Front. Mar. Sci..

[8]  Paul J. McMurdie,et al.  Exact sequence variants should replace operational taxonomic units in marker-gene data analysis , 2017, The ISME Journal.

[9]  C. Baker-Austin,et al.  Comparison of toxR and tlh based PCR assays for Vibrio parahaemolyticus , 2017 .

[10]  J. Oliver,et al.  Different abundance and correlational patterns exist between total and presumed pathogenic Vibrio vulnificus and V. parahaemolyticus in shellfish and waters along the North Carolina coast , 2017, FEMS microbiology ecology.

[11]  Jasmine Chong,et al.  MicrobiomeAnalyst: a web-based tool for comprehensive statistical, visual and meta-analysis of microbiome data , 2017, Nucleic Acids Res..

[12]  Seung Chul Shin,et al.  The genome of the Antarctic-endemic copepod, Tigriopus kingsejongensis , 2017, GigaScience.

[13]  J. Triñanes,et al.  Non-Cholera Vibrios: The Microbial Barometer of Climate Change. , 2017, Trends in microbiology.

[14]  R. Colwell,et al.  Climate influence on Vibrio and associated human diseases during the past half-century in the coastal North Atlantic , 2016, Proceedings of the National Academy of Sciences.

[15]  J. Fuhrman,et al.  Every base matters: assessing small subunit rRNA primers for marine microbiomes with mock communities, time series and global field samples. , 2016, Environmental microbiology.

[16]  Paul J. McMurdie,et al.  DADA2: High resolution sample inference from Illumina amplicon data , 2016, Nature Methods.

[17]  L. Fu,et al.  Chitinase producing bacteria with direct algicidal activity on marine diatoms , 2016, Scientific Reports.

[18]  R. Burton,et al.  Reverse genetics in the tide pool: knock‐down of target gene expression via RNA interference in the copepod Tigriopus californicus , 2015, Molecular ecology resources.

[19]  J. Oliver,et al.  Molecular and Physical Factors That Influence Attachment of Vibrio vulnificus to Chitin , 2015, Applied and Environmental Microbiology.

[20]  E. Antonova,et al.  Genetics of Natural Competence in Vibrio cholerae and other Vibrios. , 2015, Microbiology spectrum.

[21]  K. Coyne,et al.  Community-Level and Species-Specific Associations between Phytoplankton and Particle-Associated Vibrio Species in Delaware's Inland Bays , 2015, Applied and Environmental Microbiology.

[22]  Chang-hoon Kim,et al.  Isolation and Physiological Characterization of a Novel Algicidal Virus Infecting the Marine Diatom Skeletonema costatum , 2015, The plant pathology journal.

[23]  J. Oliver The Biology of Vibrio vulnificus , 2015, Microbiology spectrum.

[24]  D. McDougald,et al.  Interactions of Vibrio spp. with Zooplankton , 2015, Microbiology spectrum.

[25]  Guizhong Wang,et al.  Pelagic microalgae as suitable diets for the benthic harpacticoid copepod Tigriopus japonicus , 2015, Hydrobiologia.

[26]  Bradd J. Haley,et al.  Deep-sea hydrothermal vent bacteria related to human pathogenic Vibrio species , 2015, Proceedings of the National Academy of Sciences.

[27]  S. Levy Warming Trend: How Climate Shapes Vibrio Ecology , 2015, Environmental health perspectives.

[28]  M. Blokesch,et al.  The type VI secretion system of Vibrio cholerae fosters horizontal gene transfer , 2015, Science.

[29]  E. Lipp,et al.  Detection of Vibrio parahaemolyticus, Vibrio vulnificus and Vibrio cholerae with respect to seasonal fluctuations in temperature and plankton abundance. , 2014, Environmental microbiology.

[30]  J. Vieites,et al.  In-house validation of novel multiplex real-time PCR gene combination for the simultaneous detection of the main human pathogenic vibrios (Vibrio cholerae, Vibrio parahaemolyticus, and Vibrio vulnificus) , 2014 .

[31]  Alison F. Takemura,et al.  Associations and dynamics of Vibrionaceae in the environment, from the genus to the population level , 2013, Front. Microbiol..

[32]  D. McDougald,et al.  Environmental reservoirs and mechanisms of persistence of Vibrio cholerae , 2013, Front. Microbiol..

[33]  B. Hammer,et al.  Competence and natural transformation in vibrios , 2013, Molecular microbiology.

[34]  K. Frischkorn,et al.  Vibrio parahaemolyticus type IV pili mediate interactions with diatom-derived chitin and point to an unexplored mechanism of environmental persistence. , 2013, Environmental microbiology.

[35]  Susan Holmes,et al.  phyloseq: An R Package for Reproducible Interactive Analysis and Graphics of Microbiome Census Data , 2013, PloS one.

[36]  Pelin Yilmaz,et al.  The SILVA ribosomal RNA gene database project: improved data processing and web-based tools , 2012, Nucleic Acids Res..

[37]  Stéphane Audic,et al.  The Protist Ribosomal Reference database (PR2): a catalog of unicellular eukaryote Small Sub-Unit rRNA sequences with curated taxonomy , 2012, Nucleic Acids Res..

[38]  E. Alm,et al.  Shape and evolution of the fundamental niche in marine Vibrio , 2012, The ISME Journal.

[39]  C. Baker-Austin,et al.  pilF polymorphism-based real-time PCR to distinguish Vibrio vulnificus strains of human health relevance. , 2012, Food microbiology.

[40]  I. Karunasagar,et al.  Water column dynamics of Vibrio in relation to phytoplankton community composition and environmental conditions in a tropical coastal area. , 2011, Environmental microbiology.

[41]  R. Colwell,et al.  Role of Zooplankton Diversity in Vibrio cholerae Population Dynamics and in the Incidence of Cholera in the Bangladesh Sundarbans , 2011, Applied and Environmental Microbiology.

[42]  G. Pohnert,et al.  Interactions of the Algicidal Bacterium Kordia algicida with Diatoms: Regulated Protease Excretion for Specific Algal Lysis , 2011, PloS one.

[43]  H. Grossart,et al.  Growth and release of extracellular organic compounds by benthic diatoms depend on interactions with bacteria. , 2011, Environmental microbiology.

[44]  C. Baker-Austin,et al.  Rapid in situ detection of virulent Vibrio vulnificus strains in raw oyster matrices using real-time PCR. , 2009, Environmental microbiology reports.

[45]  Francisco J. Roig,et al.  pilF Polymorphism-Based PCR To Distinguish Vibrio vulnificus Strains Potentially Dangerous to Public Health , 2009, Applied and Environmental Microbiology.

[46]  Katherine H. Phillippy,et al.  Whole-genome microarray analyses of Synechococcus-Vibrio interactions. , 2009, Environmental microbiology.

[47]  Susan M. Huse,et al.  A Method for Studying Protistan Diversity Using Massively Parallel Sequencing of V9 Hypervariable Regions of Small-Subunit Ribosomal RNA Genes , 2009, PloS one.

[48]  Thomas Mock,et al.  Chitin in Diatoms and Its Association with the Cell Wall , 2009, Eukaryotic Cell.

[49]  E. Lipp,et al.  Plankton composition and environmental factors contribute to Vibrio seasonality , 2009, The ISME Journal.

[50]  R. Colwell,et al.  Association of Vibrio cholerae with plankton in coastal areas of Mexico. , 2009, Environmental microbiology.

[51]  Lawrence A. David,et al.  Resource Partitioning and Sympatric Differentiation Among Closely Related Bacterioplankton , 2008, Science.

[52]  V. Martin‐Jézéquel,et al.  Contribution of multi-nuclear solid state NMR to the characterization of the Thalassiosira pseudonana diatom cell wall , 2008, Analytical and bioanalytical chemistry.

[53]  N. Jiao,et al.  Isolation and characterization of a marine algicidal bacterium against the toxic dinoflagellate Alexandrium tamarense , 2007 .

[54]  R. Colwell,et al.  Association of Vibrio cholerae O1 El Tor and O139 Bengal with the Copepods Acartia tonsa and Eurytemora affinis , 2007, Applied and Environmental Microbiology.

[55]  D. Gevers,et al.  Conservation of the Chitin Utilization Pathway in the Vibrionaceae , 2007, Applied and Environmental Microbiology.

[56]  Maureen A. O’Malley The nineteenth century roots of 'everything is everywhere' , 2007, Nature Reviews Microbiology.

[57]  H. Grossart,et al.  Interactions of planktonic algae and bacteria: effects on algal growth and organic matter dynamics , 2007 .

[58]  Ryan S. Mueller,et al.  Vibrio cholerae Strains Possess Multiple Strategies for Abiotic and Biotic Surface Colonization , 2007, Journal of bacteriology.

[59]  J. Town,et al.  Improved template representation in cpn60 polymerase chain reaction (PCR) product libraries generated from complex templates by application of a specific mixture of PCR primers. , 2006, Environmental microbiology.

[60]  Gábor Csárdi,et al.  The igraph software package for complex network research , 2006 .

[61]  G. Schoolnik,et al.  Chitin Induces Natural Competence in Vibrio cholerae , 2005, Science.

[62]  Rita R. Colwell,et al.  Critical Factors Influencing the Occurrence of Vibrio cholerae in the Environment of Bangladesh , 2005, Applied and Environmental Microbiology.

[63]  H. Grossart,et al.  Marine diatom species harbour distinct bacterial communities. , 2005, Environmental microbiology.

[64]  J. Oliver Wound infections caused by Vibrio vulnificus and other marine bacteria , 2005, Epidemiology and Infection.

[65]  G. Donelli,et al.  Pathogenic Vibrio Species in the Marine and Estuarine Environment , 2005 .

[66]  S. Penny,et al.  cpnDB: a chaperonin sequence database. , 2004, Genome research.

[67]  Farooq Azam,et al.  Algicidal Bacteria in the Sea and their Impact on Algal Blooms1 , 2004, The Journal of eukaryotic microbiology.

[68]  S. County County of San Diego Health and Human Services Agency Emergency Medical Services , 2004 .

[69]  A. Wright,et al.  Real-Time PCR Analysis of Vibrio vulnificus from Oysters , 2003, Applied and Environmental Microbiology.

[70]  Rita R. Colwell,et al.  Effects of Global Climate on Infectious Disease: the Cholera Model , 2002, Clinical Microbiology Reviews.

[71]  D. Maneval,et al.  A bacteriophage encoding a pathogenicity island, a type-IV pilus and a phage receptor in cholera bacteria , 1999, Nature.

[72]  Rita R. Colwell Global Climate and Infectious Disease: The Cholera Paradigm* , 1996, Science.

[73]  Jeffery R Cordell,et al.  The invasive Asian copepodPseudodiaptomus inopinus in Oregon, Washington, and British Columbia estuaries , 1996 .

[74]  P. Wangersky,et al.  Production of dissolved organic carbon in phyloplankton cultures as measured by high-temperature catalytic oxidation and ultraviolet photo-oxidation methods , 1996 .

[75]  R. Reynolds,et al.  HSP60 gene sequences as universal targets for microbial species identification: studies with coagulase-negative staphylococci , 1996, Journal of clinical microbiology.

[76]  M. Tamplin,et al.  Effects of temperature and salinity on the survival of Vibrio vulnificus in seawater and shellfish , 1993, Applied and environmental microbiology.

[77]  R. R. Colwell,et al.  Viable but Non-Culturable Vibrio cholerae and Related Pathogens in the Environment: Implications for Release of Genetically Engineered Microorganisms , 1985, Bio/Technology.

[78]  R. Colwell,et al.  Ecological relationships between Vibrio cholerae and planktonic crustacean copepods , 1983, Applied and environmental microbiology.

[79]  R. Colwell,et al.  Adsorption of Vibrio parahaemolyticus onto chitin and copepods. , 1975, Applied microbiology.

[80]  C. Lorenzen,et al.  Fluorometric Determination of Chlorophyll , 1965 .