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

Tarazona-Janampa, Ulrike I.; Cembella, Allan; Pelayo-Zárate, María C.; Pajares, Silvia; Márquez-Valdelamar, Laura; Okolodkov, Yuri B.; Tebben, Jan; Krock, Bernd; Durán-Riveroll, Lorena M.

doi:10.3389/fmars.2020.00569

Cited by 20 publications

(37 citation statements)

References 60 publications

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“…The differences of chemical alteration between axenic or xenic P. lima conditions clearly emphasize the effect of associated bacteria in the fungal/microalgal interaction (Figure 2). Interactions between P. lima and bacteria were shown to alter algal metabolites [68], and it is thus expected that in the present study the bacterial presence also significantly impacted the metabolite profile. Finally, this showed that, in addition to dinoflagellate signals, the microbiome metabolism is also altered.…”

Section: Discussionmentioning

confidence: 74%

Deciphering microbiome impacts on fungal-microalgal interaction in a marine environment using metabolomics

Berry

Briand

Bagot

et al. 2021

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The comprehension of microbial interactions is one of the key challenges in microbial ecology. The present study focuses on studying the chemical interaction between the toxic dinoflagellate Prorocentrum lima PL4V strain and associated fungal strains (two Penicillium sp. strains and three Aspergillus sp) among which the Aspergillus pseudoglaucus strain MMS1589 was selected for further co-culture experiment. Such rarely studied interaction (fungal-microalgal) was explored in axenic and non-axenic conditions, in a dedicated microscale marine environment (hybrid solid/liquid conditions), to delineate specialized metabolome alteration in relation to the P. lima and A. pseudoglaucus co-culture in regard to the presence of their associated bacteria. Such alteration was monitored by high-performance liquid chromatography coupled to high-resolution mass spectrometry (LC-HRMS). In-depth analysis of the resulting data highlighted (1) the chemical modification associated to fungal-microalgal co-culture, and (2) the impact of associated bacteria in microalgal resilience to fungal interaction. Even if only a very low number of highlighted metabolites were fully characterised due to the poor chemical investigation of the studied species, a clear co-culture induction of the dinoflagellate toxins okadaic acid and dinophysistoxin 1 was observed. Such results highlight the importance to consider microalgal microbiome to study parameters regulating toxin production. Finally, a microscopic observation showed an unusual physical interaction between the fungal mycelium and the dinoflagellates.

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Section: Discussionmentioning

confidence: 74%

Deciphering microbiome impacts on fungal-microalgal interaction in a marine environment using metabolomics

Berry

Briand

Bagot

et al. 2021

Preprint

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“…Harvest details of actively growing Prorocentrum cultures and cell enumeration for DSP toxin analysis followed previously described methods (Tarazona-Janampa et al, 2020). In brief, cultured cells were harvested from plastic Petri plates by multiple centrifugation steps.…”

Section: Isolation and Culture Of Prorocentrummentioning

confidence: 99%

“…Nagahama et al (2011) is one of the most widely distributed species of the genus. In tropical and sub-tropical coastal ecosystems (Durán-Riveroll et al, 2019) the species is commonly found as an epiphyte upon macroalgae, seagrasses, and inanimate substrates (Tarazona-Janampa et al, 2020). There is limited and somewhat contradictory evidence of biotic substrate preferences for benthic Prorocentrum (Boisnoir et al, 2019), but little is known about the basis of the selective mechanisms, chemical ecological interactions or potential effect on toxin production or composition.…”

Section: Introductionmentioning

confidence: 99%

Phylogeography and Diversity Among Populations of the Toxigenic Benthic Dinoflagellate Prorocentrum From Coastal Reef Systems in Mexico

et al. 2021

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The marine dinoflagellate genus Prorocentrum Ehrenberg comprises many species occupying primarily benthic or epiphytic habitats, particularly in tropical and sub-tropical waters. Despite concerted efforts to establish phylogenetic associations, there remain unresolved issues in defining morphospecies and membership in species complexes. The study described herein addressed the inter- and infraspecific relationships of members of the Prorocentrum lima and Prorocentrum hoffmannianum species complexes (PLSC and PHSC, respectively) by applying multivariate approaches in morphotaxonomy, molecular phylogenetics and chemodiversity to establish affinities among multiple clonal isolates. Morphotaxonomic analysis showed consistency with classical morphospecies descriptors, and high variability in cell size and dimensions, but did not challenge current species complex concepts. Phylogenetic analysis of ITS/5.8S rDNA sequences from isolates from the Gulf of California, Caribbean Sea, and Gulf of Mexico coasts compared with archived global GenBank sequences served to define five consistent clades with separation of the PLSC and PHSC. Secondary structure modeling of ITS2 rRNA variation based on compensatory base changes (CBC) was effective in resolving details of the respective species complexes and even indicated putative incipient or cryptic speciation due to potential hybridization barriers. This study represents the largest (n = 67 isolates) chemodiversity analysis of polyketide-derived toxins associated with diarrheic shellfish poisoning (DSP) from a benthic dinoflagellate genus. Relative composition of some analogs (OA, OA-D8, DTX1, DTX1a, and DTX1a-D8), including two new undescribed isomers, distinguished P. lima from P. hoffmannianum sensu lato, but without clear associations with substrate type or geographical origin. Although all P. lima and most (one exception) P. hoffmannianum were toxigenic, the total cell toxin content could not be linked at the species level. This research demonstrates that clonal chemodiversity in toxin composition cannot yet be effectively applied to define ecological niches or species interactions within local assemblages. Phylogenetic analysis of the ITS/5.8 rDNA, particularly when combined with secondary structure modeling, rather than only a comparison of LSU rDNA sequences, is a more powerful approach to identify cryptic speciation and to resolve species complexes within benthic dinoflagellate groups.

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“…Therefore, the interaction between dinoflagellates (i.e., Prorocentrum) and their co-existing microbiome encoding the polyketide synthase gene may influence intracellular phycotoxin production (Perez et al, 2008;Lee et al, 2016). However, to date, there is little evidence that supports that extracellular bacteria influence growth and phycotoxin production (Tarazona-Janampa et al, 2020). A sound knowledge of cell cycle regulation and metabolism, synchronization of the cell cycle, use of optimum nutritional requirements and culture conditions, awareness of stress factors and optimized configurations of bioreactors are fundamental to mass culture of dinoflagellates for phycotoxin production.…”

Section: Culture Of Dinoflagellatesmentioning

confidence: 99%

High Value Phycotoxins From the Dinoflagellate Prorocentrum

et al. 2021

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Marine dinoflagellates produce chemically diverse compounds, with a wide range of biological activity (antimicrobial, anticancer, treatment of neurodegenerative disease along with use as biomedical research tools). Chemical diversity is highlighted by their production of molecules such as the saxitoxin family of alkaloids (C10H17N7O4 – 299 g/mol) to the amphipathic maitotoxin (C164H256O68S2Na2 – 3,422 g/mol), representing one of the largest and most complex secondary metabolites characterized. Dinoflagellates, are most well-known for the production of red tides which are frequently toxic, including okadaic acid and related dinophysistoxins, which are tumor promoters. The mode of action for these phycotoxins, is by specific inhibition of protein phosphatases, enzymes essential in regulation of many cellular processes. Hence, these compounds are being used for vital cell regulation studies. However, the availability of useful amounts of these compounds has restricted research. Chemical synthesis of some compounds such as okadaic acid has been investigated, but the complexity of the molecule resulted in many lengthy steps and achieved only a poor yield. The use of naturally occurring phytoplankton has been investigated as a potential source of these compounds, but it has been shown to be unreliable and impractical. The most practical option is large scale culture with down-stream processing/purification which requires specialist facilities and expertise. This review, describes the biotechnological potential of these organisms and the challenges to achieve useful yields of high quality phycotoxins using Prorocentrum spp. as an example to produce okadaic acid.

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

Cited by 20 publications

References 60 publications

Deciphering microbiome impacts on fungal-microalgal interaction in a marine environment using metabolomics

Deciphering microbiome impacts on fungal-microalgal interaction in a marine environment using metabolomics

Phylogeography and Diversity Among Populations of the Toxigenic Benthic Dinoflagellate Prorocentrum From Coastal Reef Systems in Mexico

High Value Phycotoxins From the Dinoflagellate Prorocentrum

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