Associated Bacteria and Their Effects on Growth and Toxigenicity of the Dinoflagellate Prorocentrum lima Species Complex From Epibenthic Substrates Along Mexican Coasts

The dinoflagellate genus Prorocentrum is globally represented by a wide variety of species found upon benthic and/or epiphytic substrates. Many epibenthic Prorocentrum species produce lipophilic polyether toxins, some of which act as potent protein phosphatase inhibitors and tumor-promoters associat...

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Main Authors: Ulrike I. Tarazona-Janampa, Allan D. Cembella, María C. Pelayo-Zárate, Silvia Pajares, Laura M. Márquez-Valdelamar, Yuri B. Okolodkov, Jan Tebben, Bernd Krock, Lorena M. Durán-Riveroll
Format: Article
Language:English
Published: Frontiers Media S.A. 2020-07-01
Series:Frontiers in Marine Science
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fmars.2020.00569/full
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author Ulrike I. Tarazona-Janampa
Ulrike I. Tarazona-Janampa
Ulrike I. Tarazona-Janampa
Allan D. Cembella
María C. Pelayo-Zárate
María C. Pelayo-Zárate
Silvia Pajares
Laura M. Márquez-Valdelamar
Yuri B. Okolodkov
Jan Tebben
Bernd Krock
Lorena M. Durán-Riveroll
Lorena M. Durán-Riveroll
spellingShingle Ulrike I. Tarazona-Janampa
Ulrike I. Tarazona-Janampa
Ulrike I. Tarazona-Janampa
Allan D. Cembella
María C. Pelayo-Zárate
María C. Pelayo-Zárate
Silvia Pajares
Laura M. Márquez-Valdelamar
Yuri B. Okolodkov
Jan Tebben
Bernd Krock
Lorena M. Durán-Riveroll
Lorena M. Durán-Riveroll
Associated Bacteria and Their Effects on Growth and Toxigenicity of the Dinoflagellate Prorocentrum lima Species Complex From Epibenthic Substrates Along Mexican Coasts
Frontiers in Marine Science
Prorocentrum
Diarrheic Shellfish Poisoning
bacteria
allelochemical
polyether toxins
author_facet Ulrike I. Tarazona-Janampa
Ulrike I. Tarazona-Janampa
Ulrike I. Tarazona-Janampa
Allan D. Cembella
María C. Pelayo-Zárate
María C. Pelayo-Zárate
Silvia Pajares
Laura M. Márquez-Valdelamar
Yuri B. Okolodkov
Jan Tebben
Bernd Krock
Lorena M. Durán-Riveroll
Lorena M. Durán-Riveroll
author_sort Ulrike I. Tarazona-Janampa
title Associated Bacteria and Their Effects on Growth and Toxigenicity of the Dinoflagellate Prorocentrum lima Species Complex From Epibenthic Substrates Along Mexican Coasts
title_short Associated Bacteria and Their Effects on Growth and Toxigenicity of the Dinoflagellate Prorocentrum lima Species Complex From Epibenthic Substrates Along Mexican Coasts
title_full Associated Bacteria and Their Effects on Growth and Toxigenicity of the Dinoflagellate Prorocentrum lima Species Complex From Epibenthic Substrates Along Mexican Coasts
title_fullStr Associated Bacteria and Their Effects on Growth and Toxigenicity of the Dinoflagellate Prorocentrum lima Species Complex From Epibenthic Substrates Along Mexican Coasts
title_full_unstemmed Associated Bacteria and Their Effects on Growth and Toxigenicity of the Dinoflagellate Prorocentrum lima Species Complex From Epibenthic Substrates Along Mexican Coasts
title_sort associated bacteria and their effects on growth and toxigenicity of the dinoflagellate prorocentrum lima species complex from epibenthic substrates along mexican coasts
publisher Frontiers Media S.A.
series Frontiers in Marine Science
issn 2296-7745
publishDate 2020-07-01
description The dinoflagellate genus Prorocentrum is globally represented by a wide variety of species found upon benthic and/or epiphytic substrates. Many epibenthic Prorocentrum species produce lipophilic polyether toxins, some of which act as potent protein phosphatase inhibitors and tumor-promoters associated with Diarrheic Shellfish Poisoning (DSP). Most members of the Prorocentrum lima species complex (PLSC) commonly found in the tropics and sub-tropics are toxigenic. Epiphytic and planktonic bacteria co-occur with toxigenic Prorocentrum but reciprocal allelochemical interactions are under-investigated. The aim of the present study was to identify the culturable bacteria collected together with isolates of the PLSC from seagrass (Thalassia testudinum) and macroalgae along tropical Atlantic coasts of Mexico, and to explore potential species interactions with selected isolates. Twenty-one bacterial genera belonging to Proteobacteria, Actinobacteria, and Bacteroidetes were identified by amplification of the 16S rRNA gene marker from nine clonal Prorocentrum cultures, with γ-proteobacteria comprising the dominant class. A positive correlation was found between the bacterial genera associated with two Prorocentrum clones and the esterified toxin analog DTX1a-D8, but there was no apparent correlation between the other PLSC clones and their associated bacteria with the other five DSP toxins detected. No bacteriostatic or allelochemical response was found for cell- and culture medium extracts of five Prorocentrum isolates assayed for bioactivity against Staphylococcus sp. DMBS2 and Vibrio sp. HEL66. Bulk cell-washing of Prorocentrum PA1, followed by growth with antibiotics, was only effective in reducing bacterial load in the initial growth stages, but did not yield axenic cultures or lower bacterial cell densities throughout the culture cycle. Antibiotic treatment did not impair growth or survival of the dinoflagellate, or apparently affect DSP toxin production. There was no significant correlation between Prorocentrum cell volume, growth rate, bacterial cell counts, or cellular toxin concentration over the entire time-series culture cycle. Benthic Prorocentrum and associated bacterial communities comprise highly diverse and characteristic microbiomes upon substrates, and among compartments in culture, but this study provides little evidence that allelochemical interactions among Prorocentrum cells and associated bacteria originating from epibenthic substrates play a definable role in growth and toxigenicity.
topic Prorocentrum
Diarrheic Shellfish Poisoning
bacteria
allelochemical
polyether toxins
url https://www.frontiersin.org/article/10.3389/fmars.2020.00569/full
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spelling doaj-f2797d9e7de844ef83d76590a1d064182020-11-25T03:10:52ZengFrontiers Media S.A.Frontiers in Marine Science2296-77452020-07-01710.3389/fmars.2020.00569520151Associated Bacteria and Their Effects on Growth and Toxigenicity of the Dinoflagellate Prorocentrum lima Species Complex From Epibenthic Substrates Along Mexican CoastsUlrike I. Tarazona-Janampa0Ulrike I. Tarazona-Janampa1Ulrike I. Tarazona-Janampa2Allan D. Cembella3María C. Pelayo-Zárate4María C. Pelayo-Zárate5Silvia Pajares6Laura M. Márquez-Valdelamar7Yuri B. Okolodkov8Jan Tebben9Bernd Krock10Lorena M. Durán-Riveroll11Lorena M. Durán-Riveroll12Alfred-Wegener-Institut, Helmholtz-Zentrum für Polar-und Meeresforschung, Bremerhaven, GermanyInternational Max Planck Research School, Max Planck Institute for Marine Microbiology, Bremen, GermanyLaboratorio de Microbiología Molecular y Genómica Bacteriana, Universidad Científica del Sur, Lima, PeruAlfred-Wegener-Institut, Helmholtz-Zentrum für Polar-und Meeresforschung, Bremerhaven, GermanyFacultad de Ciencias, Universidad Nacional Autónoma de México, Mexico City, MexicoInstituto de Ciencias del Mar y Limnología, Universidad Nacional Autónoma de México, Mexico City, MexicoInstituto de Ciencias del Mar y Limnología, Universidad Nacional Autónoma de México, Mexico City, MexicoLaboratorio Nacional de Biodiversidad, Instituto de Biología, Universidad Nacional Autónoma de México, Mexico City, MexicoInstituto de Ciencias Marinas y Pesquerías, Universidad Veracruzana, Veracruz, MexicoAlfred-Wegener-Institut, Helmholtz-Zentrum für Polar-und Meeresforschung, Bremerhaven, GermanyAlfred-Wegener-Institut, Helmholtz-Zentrum für Polar-und Meeresforschung, Bremerhaven, GermanyAlfred-Wegener-Institut, Helmholtz-Zentrum für Polar-und Meeresforschung, Bremerhaven, GermanyCONACyT-Departamento de Biotecnología Marina, Centro de Investigación Científica y de Educación Superior de Ensenada, Benito Juarez, MexicoThe dinoflagellate genus Prorocentrum is globally represented by a wide variety of species found upon benthic and/or epiphytic substrates. Many epibenthic Prorocentrum species produce lipophilic polyether toxins, some of which act as potent protein phosphatase inhibitors and tumor-promoters associated with Diarrheic Shellfish Poisoning (DSP). Most members of the Prorocentrum lima species complex (PLSC) commonly found in the tropics and sub-tropics are toxigenic. Epiphytic and planktonic bacteria co-occur with toxigenic Prorocentrum but reciprocal allelochemical interactions are under-investigated. The aim of the present study was to identify the culturable bacteria collected together with isolates of the PLSC from seagrass (Thalassia testudinum) and macroalgae along tropical Atlantic coasts of Mexico, and to explore potential species interactions with selected isolates. Twenty-one bacterial genera belonging to Proteobacteria, Actinobacteria, and Bacteroidetes were identified by amplification of the 16S rRNA gene marker from nine clonal Prorocentrum cultures, with γ-proteobacteria comprising the dominant class. A positive correlation was found between the bacterial genera associated with two Prorocentrum clones and the esterified toxin analog DTX1a-D8, but there was no apparent correlation between the other PLSC clones and their associated bacteria with the other five DSP toxins detected. No bacteriostatic or allelochemical response was found for cell- and culture medium extracts of five Prorocentrum isolates assayed for bioactivity against Staphylococcus sp. DMBS2 and Vibrio sp. HEL66. Bulk cell-washing of Prorocentrum PA1, followed by growth with antibiotics, was only effective in reducing bacterial load in the initial growth stages, but did not yield axenic cultures or lower bacterial cell densities throughout the culture cycle. Antibiotic treatment did not impair growth or survival of the dinoflagellate, or apparently affect DSP toxin production. There was no significant correlation between Prorocentrum cell volume, growth rate, bacterial cell counts, or cellular toxin concentration over the entire time-series culture cycle. Benthic Prorocentrum and associated bacterial communities comprise highly diverse and characteristic microbiomes upon substrates, and among compartments in culture, but this study provides little evidence that allelochemical interactions among Prorocentrum cells and associated bacteria originating from epibenthic substrates play a definable role in growth and toxigenicity.https://www.frontiersin.org/article/10.3389/fmars.2020.00569/fullProrocentrumDiarrheic Shellfish Poisoningbacteriaallelochemicalpolyether toxins