Growth and Toxin Production of Gambierdiscus spp. Can Be Regulated by Quorum-Sensing Bacteria

Abstract

Gambierdiscus spp. are the major culprit responsible for global ciguatera fish poisoning (CFP). At present, the effects of microbiological factors on algal proliferation and toxin production are poorly understood. To evaluate the regulatory roles of quorum-sensing (QS) bacteria in the physiology of Gambierdiscus, co-culture experiments with screened QS strains were conducted in this study. Except for the growth-inhibiting effect from the strain Marinobacter hydrocarbonoclasticus, the algal host generally displayed much higher growth potential and toxin production ability with the existence of QS strains. In addition, Bacillus anthracis particularly exhibited a broad-spectrum growth enhancement effect on various Gambierdiscus types, as well as a remarkable influence on algal toxicity. The variations of algal physiological status, including growth rate, chlorophyll content, and responsive behaviors, are potential reasons for the observed positive or negative affection. This study suggests that QS bacteria regulate the algal growth and toxin production. Based on the evidence, we further speculate that QS bacteria may contribute to the site-specific distribution of CFP risk through regulating the algal host biomass and toxicity.

Intraspecific Variability in the Toxin Production and Toxin Profiles of In Vitro Cultures of Gambierdiscus polynesiensis (Dinophyceae) from French Polynesia

“…The production pattern described in many Gambierdiscus species, including G. polynesiensis, clearly suggests a trade-off between reduced growth and increased toxin synthesis and poses the question of the ecological relevance of the toxins synthesized by Gambierdiscus/Fukuyoa spp. The diversity and structural complexity of ciguatera toxins have led to the speculation that allelochemical agents may be used by Gambierdiscus to compete with other epiphytic dinoflagellates for space or limit grazing by herbivores [3,24,54,69,85,86]. This hypothesis is strongly supported by the results of several studies that have examined the interactions between Gambierdiscus spp.…”

“…Results point out the complexity of the toxinogenesis in Gambierdiscus/Fukuyoa spp. and suggest that this functional trait may be under the control of a combination of factors, including genetic [15,54,65,66], physiological [24,65,67], environmental [43,68] and microbial drivers [69]. These variations in Gambierdiscus/Fukuyoa species/strains affect not only the nominal cell toxin content but may also concern the toxin profiles, i.e., both the identity and ratio of the different CTXs congeners produced [24,50].…”

Ciguatera Fish Poisoning: The Risk from an Aotearoa/New Zealand Perspective

“…The data indicate that nothing is simple, and while there is the real possibility that warming waters will favour Gambierdiscus growth (as indicated by the correlation between the Southern Oscillation Index and increased CFP cases), large bodies of extremely warm water, which last for extended periods, as in the Indo-Pacific Warm Pool, may depress CFP rates [107]. To complicate things even further, quorum-sensing bacteria have been shown to impact the growth and toxin production of Gambierdiscus [107], and the effects of climate change on associated bacterial species, and thus on CFP, can only be speculated on at this time.…”

Ciguatera Mini Review: 21st Century Environmental Challenges and the Interdisciplinary Research Efforts Rising to Meet Them

“…In culture, Gambierdiscus has displayed inter- and intra-species variability for growth, morphology, and quali-quantitative toxin profile [ 83 , 104 ], which can be influenced by capture location, culture parameters, and time spent in culture (phycological drift) [ 20 , 73 , 74 , 75 , 104 , 105 , 106 , 107 , 108 ]. Interactions between bacterial or other microbial co-inhabitants and Gambierdiscus indicated antagonism, competition, or benefits with impacts on fitness and bi-directional regulation in compound production [ 109 , 110 , 111 ]. From the perspective of the algae, it remains undescribed whether CTXs, MTXs, and other known compounds (e.g., gambierone, gambieric acids) are produced for inter- or intra-species defense or benefit.…”