Microbiome Associated With Gambierdiscus balechii Cultures Under Different Toxicity Conditions

Abstract

Dinoflagellates, including harmful algal bloom species, are known to co-exist with and rely upon bacteria but how the microbiome changes with the physiologies of the cognate dinoflagellates is poorly understood. Here, we used 16S rRNA gene meta-barcoding to characterize the bacterial community in the cultures of Gambierdiscus balechii, a ciguatoxin-producing benthic dinoflagellate, under different nitrogen (N)-nutrient conditions and at different ciguatoxin-producing growth. The high-throughput sequencing of a total of 12 libraries generated 926,438 reads which were classified into 16 phyla. We observed a shift of the G. balechii-associated microbiome from N-replete to low-N conditions and from the early (low toxin) to the late exponential (high toxin) growth stage. Common across these conditions were species from families Rhodobacteraceae and Flavobacteriaceae. Species abundant in the low-N condition mainly included Planctomyces, Ekhidna, and Lactobacillus. Dominant or highly abundant microbial taxa in the high toxin-producing stage (N-replete, late exponential stage) were Oceanococcus and Marinoscillum. Under this condition, one Rhizobiales bacterium, Oricola, also increased in relative abundance. Our study documents the high diversity and dynamics of the G. balechii-associated microbiome, and identifies condition-specific sub-communities: the core (constitutive) microbiome that stably co-exists with G. balechii, the bacterial lineages that are responsive to N-nutrient variations, and species whose abundances are correlated with toxin content of the dinoflagellate. These findings demonstrate that particular bacterial groups are responsive to N-nutrient or toxicity changes of G. balechii and thus will be useful for further investigations on the associated microbiome’s interactions with benthic dinoflagellates and functions in the course of benthic harmful algae blooms.

Identification and implications of a core bacterial microbiome in 19 clonal cultures laboratory-reared for months to years of the cosmopolitan dinoflagellate Karlodinium veneficum

“…The whole bacterial microbiome of K. veneficum recovered in our study was generally congruent with the majority of previously characterized bacterial assemblages associated with laboratory cultures of dinoflagellates, in which αand γ-proteobacteria are the predominant players (Li et al, 2019;Guo et al, 2020;Tarazona-Janampa et al, 2020;Deng et al, 2022;Wu et al, 2022;and the references therein). Despite the heterogeneity of feature composition, bacterial communities of strains from different geographic origins consisted a core set of constitutive taxa.…”

“…Despite the heterogeneity of feature composition, bacterial communities of strains from different geographic origins consisted a core set of constitutive taxa. Among them, the Alteromonas and Marinobacter (Alteromonadaceae) are the dominant phylotypes ubiquitously associated with a wide variety of dinoflagellates in both laboratory cultures and field samples (Mayali et al, 2011;Yang et al, 2015;Bolch et al, 2017;Park et al, 2018;Shin et al, 2018;Zhou et al, 2018;Hattenrath-Lehmann et al, 2019;Li et al, 2019;Cui et al, 2020;Guo et al, 2020;Tarazona-Janampa et al, 2020;Kang et al, 2021;Deng et al, 2022;Wu et al, 2022). Metabolically active Marinobacter may be essential for trace metal uptake of dinoflagellates via a beneficial interaction process well known as Iron-Carbon mutualism (Amin et al, 2009).…”

“…In this study, bacterial taxa that were commonly and abundantly present across different samples were regarded as the core or stable constituents of the dinoflagellate-associated microbiome, a definition similarly adopted in the previous works on dinoflagellates (Lawson et al, 2018;Sörenson et al, 2019;Maire et al, 2021;Wu et al, 2022). Hence, the core microbiome was defined hereafter as those taxa present in 100% of all samples with a minimum relative abundance of 0.1%.…”

“…With the ever-increasing number of dinoflagellate HAB events worldwide in the past decades, the importance of dinoflagellatebacteria interactions have been increasingly emphasized due to amassed evidence of linkages between bacterioplankton and the population dynamics of dinoflagellates in the blooming field (Mayali et al, 2011;Yang et al, 2015;Zhou et al, 2018;Hattenrath-Lehmann et al, 2019;Cui et al, 2020;Kang et al, 2021;Maire et al, 2021). Meanwhile, bacteria within certain lineages (e.g., Roseobacter clade in α-proteobacteria, Marinobacter and Alteromonas clades in γ-proteobacteria) have been commonly found both in the phycospheres of laboratory-cultured dinoflagellates (Bolch et al, 2017;Park et al, 2018;Shin et al, 2018;Li et al, 2019;Guo et al, 2020;Tarazona-Janampa et al, 2020;Deng et al, 2022;Wu et al, 2022) and field samples during dinoflagellate blooms (Mayali et al, 2011;Yang et al, 2015;Zhou et al, 2018;Hattenrath-Lehmann et al, 2019;Cui et al, 2020;Kang et al, 2021), implying that specific interactions could be established between dinoflagellates and particular groups of bacteria. However, the relationships between phytoplankton and surrounding bacteria are intimate, complex, and dynamic (Amin et al, 2012;Behringer et al, 2018;Tarazona-Janampa et al, 2020;Maire et al, 2021;Wu et al, 2022).…”

“…Meanwhile, bacteria within certain lineages (e.g., Roseobacter clade in α-proteobacteria, Marinobacter and Alteromonas clades in γ-proteobacteria) have been commonly found both in the phycospheres of laboratory-cultured dinoflagellates (Bolch et al, 2017;Park et al, 2018;Shin et al, 2018;Li et al, 2019;Guo et al, 2020;Tarazona-Janampa et al, 2020;Deng et al, 2022;Wu et al, 2022) and field samples during dinoflagellate blooms (Mayali et al, 2011;Yang et al, 2015;Zhou et al, 2018;Hattenrath-Lehmann et al, 2019;Cui et al, 2020;Kang et al, 2021), implying that specific interactions could be established between dinoflagellates and particular groups of bacteria. However, the relationships between phytoplankton and surrounding bacteria are intimate, complex, and dynamic (Amin et al, 2012;Behringer et al, 2018;Tarazona-Janampa et al, 2020;Maire et al, 2021;Wu et al, 2022). Compared with microbiota of sessile plants, the bacterial consortia co-existed with phytoplankton in aquatic habitats are particularly difficult to be accurately defined, owing to the majority of microalgae being unicellular organisms living in constantly changing and dynamic environments (Behringer et al, 2018).…”