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Distribution, abundance and diversity of Gambierdiscus spp. from a ciguatera endemic area in Marakei, Republic of Kiribati (2014)

Xu, Yixiao ; Richlen, Mindy L. ; Morton, Steve L. ; [et al.]

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Publication Date: 2022-05-25

Description: Author Posting. © The Author(s), 2014. This is the author's version of the work. It is posted here by permission of Elsevier for personal use, not for redistribution. The definitive version was published in Harmful Algae 34 (2014): 56–68, doi:10.1016/j.hal.2014.02.007.

Description: Ciguatera is a serious seafood poisoning syndrome caused by the consumption of ciguatoxin-contaminated finfish from tropical and subtropical regions. This study examined the community structure of ciguatera-associated dinoflagellates and the distribution pattern, taxonomy and toxicity of Gambierdiscus spp. from a high-risk area of Marakei, Republic of Kiribati. The genera Gambierdiscus, Prorocentrum, Ostreopsis, Amphidinium and Coolia were present, and generally the former three dominated the dinoflagellate assemblage. Among these three, Gambierdiscus was the most abundant dinoflagellate genus observed at three of the four sites sampled, two of which (Sites 1 and 2) were on the northern half of the island and two (Sites 3 and 4) on the southern half. The following patterns of abundance were observed among sites: (1) Average Gambierdiscus spp. abundance at the northern sites exceeded the southern sites by a factor of 19-54; and (2) Gambierdiscus spp. abundance at shallow sites (2-3 m) exceeded deeper sites (10-15 m). The distribution of Gambierdiscus spp. at Marakei corresponded with previously observed patterns of fish toxicity, with fish from southern locations being much less toxic than fish sampled north of the central channel. DNA sequencing identified three Gambierdiscus species (G. carpenteri, G. belizeanus, G. pacificus) and three previously unreported ribotypes (Gambierdiscus sp. type 4, Gambierdiscus sp. type 5, Gambierdiscus sp. type 6) in the samples; Gambierdiscus sp. type 4 may represent a Pacific clade of Gambierdiscus sp. ribotype 1. Toxicity analyses determined that Gambierdiscus sp. type 4 isolates were more toxic than the Gambierdiscus sp. type 5 and G. pacificus isolates, with toxin contents of 2.6-6.0 (mean: 4.3± 1.4), 0.010 and 0.011 fg P-CTX-1 eq cell-1, respectively. Despite low densities of Gambierdiscus spp. observed at Marakei relative to other studies in other parts of the world, the presence of low and moderately toxic populations may be sufficient to render the western coast of Marakei a high-risk area for ciguatera. The long history of toxicity along the western side of Marakei suggests that large-scale oceanographic forcings that regulate the distribution of Gambierdiscus spp. along the western side of Marakei may have remained relatively stable over that time. Chronic as well as acute exposure to ciguatoxins may therefore pose an important human health impact to the residents of Marakei.

Description: Funding for this work was provided by the Centers for Disease Control and Prevention (U01 EH000421), USFDA (F223201000060C), NOAA NOS (Cooperative Agreement NA11NOS4780060, NA11NOS4780028), National Program on Key Basic Research Project of China (973 Program, 2013CB956503), the Nonprofit Research Project for the State Oceanic Administration (China, 201005006-01), and the National Natural Science Foundation of China (41276110).

Keywords: Ciguatera fish poisoning ; Ciguatoxins ; Gambierdiscus ; Ostreopsis ; HABs ; Kiribati

Repository Name: Woods Hole Open Access Server

Type: Preprint

Format: application/pdf

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Influence of environmental variables on Gambierdiscus spp. (Dinophyceae) growth and distribution (2016)

Xu, Yixiao ; Richlen, Mindy L. ; Liefer, Justin D. ; [et al.]

Public Library of Science

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Publication Date: 2022-05-25

Description: © The Author(s), 2016. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in PLoS One 11 (2016): e0153197, doi:10.1371/journal.pone.0153197.

Description: Benthic dinoflagellates in the genus Gambierdiscus produce the ciguatoxin precursors responsible for the occurrence of ciguatera toxicity. The prevalence of ciguatera toxins in fish has been linked to the presence and distribution of toxin-producing species in coral reef ecosystems, which is largely determined by the presence of suitable benthic habitat and environmental conditions favorable for growth. Here using single factor experiments, we examined the effects of salinity, irradiance, and temperature on growth of 17 strains of Gambierdiscus representing eight species/phylotypes (G. belizeanus, G. caribaeus, G. carolinianus, G. carpenteri, G. pacificus, G. silvae, Gambierdiscus sp. type 4–5), most of which were established from either Marakei Island, Republic of Kiribati, or St. Thomas, United States Virgin Island (USVI). Comparable to prior studies, growth rates fell within the range of 0–0.48 divisions day-1. In the salinity and temperature studies, Gambierdiscus responded in a near Gaussian, non-linear manner typical for such studies, with optimal and suboptimal growth occurring in the range of salinities of 25 and 45 and 21.0 and 32.5°C. In the irradiance experiment, no mortality was observed; however, growth rates at 55μmol photons · m-2 · s-1 were lower than those at 110–400μmol photons · m-2 · s-1. At the extremes of the environmental conditions tested, growth rates were highly variable, evidenced by large coefficients of variability. However, significant differences in intraspecific growth rates were typically found only at optimal or near-optimal growth conditions. Polynomial regression analyses showed that maximum growth occurred at salinity and temperature levels of 30.1–38.5 and 23.8–29.2°C, respectively. Gambierdiscus growth patterns varied among species, and within individual species: G. belizeanus, G. caribaeus, G. carpenteri, and G. pacificus generally exhibited a wider range of tolerance to environmental conditions, which may explain their broad geographic distribution. In contrast, G. silvae and Gambierdiscus sp. types 4–5 all displayed a comparatively narrow range of tolerance to temperature, salinity, and irradiance.

Description: This study was funded by the National Natural Science Foundation of China (41506137); Guangxi Natural Science Foundation (2015GXNSFCA139003), Centers for Disease Control and Prevention (U01 EH000421); USFDA (F223201000060C); NOAA NOS through the CiguaHAB program (Cooperative Agreement NA11NOS4780060, NA11NOS4780028); the Lana Vento Trust and VI-EPSCoR Program (NSF award # 346483 & 081441); and a System Fund from Key Laboratory of Environment Change and Resources Use in Beibu Gulf, Ministry of Education (2014BGERLXT01). Support was also provided by the Woods Hole Center for Oceans and Human Health through National Science Foundation (NSF) Grant OCE-1314642, National Institute of Environmental Health Sciences (NIEHS) Grant 1-P01-ES021923-014, as well as the China Scholarship Council.

Repository Name: Woods Hole Open Access Server

Type: Article

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Asynchrony of Gambierdiscus spp. abundance and toxicity in the U.S. Virgin Islands: implications for monitoring and management of Ciguatera (2021)

Liefer, Justin D. ; Richlen, Mindy L. ; Smith, Tyler B. ; [et al.]

MDPI

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Publication Date: 2022-05-27

Description: © The Author(s), 2021. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Liefer, J. D., Richlen, M. L., Smith, T. B., DeBose, J. L., Xu, Y., Anderson, D. M., & Robertson, A. Asynchrony of Gambierdiscus spp. abundance and toxicity in the U.S. Virgin Islands: implications for monitoring and management of Ciguatera. Toxins, 13(6), (2021): 413, https://doi.org/10.3390/toxins13060413.

Description: Ciguatera poisoning (CP) poses a significant threat to ecosystem services and fishery resources in coastal communities. The CP-causative ciguatoxins (CTXs) are produced by benthic dinoflagellates including Gambierdiscus and Fukuyoa spp., and enter reef food webs via grazing on macroalgal substrates. In this study, we report on a 3-year monthly time series in St. Thomas, US Virgin Islands where Gambierdiscus spp. abundance and Caribbean-CTX toxicity in benthic samples were compared to key environmental factors, including temperature, salinity, nutrients, benthic cover, and physical data. We found that peak Gambierdiscus abundance occurred in summer while CTX-specific toxicity peaked in cooler months (February–May) when the mean water temperatures were approximately 26–28 °C. These trends were most evident at deeper offshore sites where macroalgal cover was highest year-round. Other environmental parameters were not correlated with the CTX variability observed over time. The asynchrony between Gambierdiscus spp. abundance and toxicity reflects potential differences in toxin cell quotas among Gambierdiscus species with concomitant variability in their abundances throughout the year. These results have significant implications for monitoring and management of benthic harmful algal blooms and highlights potential seasonal and highly-localized pulses in reef toxin loads that may be transferred to higher trophic levels.

Description: This work was funded in part by the National Oceanic and Atmospheric Administration, Ecology and Oceanography of Harmful Algal Blooms Program (ECOHAB publication number 984) through the CiguaHAB project (NA11NOS4780028), and also contributes to CIGUATOX (NA17NOS4780181) granted to coauthors AR, TBS, DMA, and MLR. Additional support was provided by NSF Partnerships in International Research and Education (1743802), and the Greater Caribbean Center for Ciguatera Research (NIH 1P01ES028949-01 and NSF 1841811). Financial support of YX was from the National Natural Science Foundation of China (41976155), the Natural Science Foundation of Guangxi Province (2020GXNSFDA297001).

Keywords: Gambierdiscus ; ciguatera poisoning ; Dictyota ; ciguatoxin ; Caribbean ; dinoflagellate ; benthic algae ; algal toxin ; harmful algal bloom

Repository Name: Woods Hole Open Access Server

Type: Article

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LSU rDNA based RFLP assays for the routine identification of Gambierdiscus species (2017)

Lyu, Yihua ; Richlen, Mindy L. ; Sehein, Taylor R. ; [et al.]

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Publication Date: 2022-05-26

Description: © The Author(s), 2017. This is the author's version of the work. It is posted here under a nonexclusive, irrevocable, paid-up, worldwide license granted to WHOI. It is made available for personal use, not for redistribution. The definitive version was published in Harmful Algae 66 (2017): 20-28, doi:10.1016/j.hal.2017.04.009.

Description: Gambierdiscus is a genus of benthic dinoflagellates commonly associated with ciguatera fish poisoning (CFP), which is generally found in tropical or sub-tropical regions around the world. Morphologically similar species within the genus can vary in toxicity; however, species identifications are difficult or sometimes impossible using light microscopy. DNA sequencing of ribosomal RNA genes (rDNA) is thus often used to identify and describe Gambierdiscus species and ribotypes, but the expense and time can be prohibitive for routine culture screening and/or large-scale monitoring programs. This study describes a restriction fragment length polymorphism (RFLP) typing method based on analysis of the large subunit ribosomal RNA gene (rDNA) that can successfully identify at least nine of the described Gambierdiscus species and two Fukuyoa species. The software programs DNAMAN 6.0 and Restriction Enzyme Picker were used to identify a set of restriction enzymes (SpeI, HpyCH4IV, and TaqαI) capable of distinguishing most of the known Gambierdiscus species for which DNA sequences were available. This assay was tested using in silico analysis and cultured isolates, and species identifications of isolates assigned by RFLP typing were confirmed by DNA sequencing. To verify the assay and assess intra-specific heterogeneity in RFLP patterns, identifications of 63 Gambierdiscus isolates comprising ten Gambierdiscus species, one ribotype, and two Fukuyoa species were confirmed using RFLP typing, and this method was subsequently employed in the routine identification of isolates collected from the Caribbean Sea. The RFLP assay presented here reduces the time and cost associated with morphological identification via scanning electron microscopy and/or DNA sequencing, and provides a phylogenetically sensitive method for routine Gambierdiscus species assignment.

Description: Funding for this study was provided by the U.S. National Oceanic and Atmospheric Administration ECOHAB program (CiguaHAB; Cooperative Agreement NA11NOS4780060, NA11NOS4780028), the China Scholarship Council and Natural Science Foundation of China (No. 41606137, 41606136), and the Guangxi Natural Science Foundation (2015GXNSFCA139003, 2016GXNSFBA380037).

Keywords: Gambierdiscus ; Ciguatera ; RFLP ; LSU rDNA

Repository Name: Woods Hole Open Access Server

Type: Preprint

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Molecular identification and toxin analysis of Alexandrium spp. in the Beibu Gulf: first report of toxic A. tamiyavanichii in Chinese coastal waters (2021)

Xu, Yixiao ; He, Xilin ; Li, Huiling ; [et al.]

MDPI

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Publication Date: 2022-05-26

Description: © The Author(s), 2021. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Xu, Y., He, X., Li, H., Zhang, T., Lei, F., Gu, H., & Anderson, D. M. Molecular identification and toxin analysis of Alexandrium spp. in the Beibu Gulf: first report of toxic A. tamiyavanichii in Chinese coastal waters. Toxins, 13(2), (2021): 161, https://doi.org/10.3390/toxins13020161.

Description: The frequency of harmful algal blooms (HABs) has increased in China in recent years. Information about harmful dinoflagellates and paralytic shellfish toxins (PSTs) is still limited in China, especially in the Beibu Gulf, where PSTs in shellfish have exceeded food safety guidelines on multiple occasions. To explore the nature of the threat from PSTs in the region, eight Alexandrium strains were isolated from waters of the Beibu Gulf and examined using phylogenetic analyses of large subunit (LSU) rDNA, small subunit (SSU) rDNA, and internal transcribed spacer (ITS) sequences. Their toxin composition profiles were also determined using liquid chromatography-tandem mass spectrometry (LC-MS/MS). All eight strains clustered in the phylogenetic tree with A. pseudogonyaulax, A. affine, and A. tamiyavanichii from other locations, forming three well-resolved groups. The intraspecific genetic distances of the three Alexandrium species were significantly smaller than interspecific genetic distances for Alexandrium species. Beibu Gulf isolates were therefore classified as A. pseudogonyaulax, A. affine, and A. tamiyavanichii. No PSTs were identified in A. pseudogonyaulax, but low levels of gonyautoxins (GTXs) 1 to 5, and saxitoxin (STX) were detected in A. tamiyavanichii (a total of 4.60 fmol/cell). The extremely low level of toxicity is inconsistent with PST detection above regulatory levels on multiple occasions within the Beibu Gulf, suggesting that higher toxicity strains may occur in those waters, but were unsampled. Other explanations including biotransformation of PSTs in shellfish and the presence of other PST-producing algae are also suggested. Understanding the toxicity and phylogeny of Alexandrium species provides foundational data for the protection of public health in the Beibu Gulf region and the mitigation of HAB events.

Description: This research was funded by the National Natural Science Foundation of China (41976155, 41506137), the Natural Science Foundation of Guangxi Province (2020GXNSFDA297001, 2016GXNSFBA380037), the Woods Hole Center for Oceans and Human Health (National Science Foundation grant OCE-1840381 and National Institutes of Health grants NIEHS-1P01-ES028938-01), the Opening Project of Guangxi Laboratory on the Study of Coral Reefs in the South China Sea (GXLSCRSCS2019002), the Opening Foundation of Key Laboratory of Environment Change and Resources Use in Beibu Gulf Ministry of Education (Nanning Normal University), and the Guangxi Key Laboratory of Earth Surface Processes and Intelligent Simulation (Nanning Normal University) (GTEU-KLOP-K1803).

Keywords: Alexandrium tamiyavanichii ; paralytic shellfish poisoning ; molecular identification ; toxicity ; harmful algal blooms ; Beibu Gulf

Repository Name: Woods Hole Open Access Server

Type: Book

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