Metabolomic Insights of the Effects of Bacterial Algicide IRI-160AA on Dinoflagellate Karlodinium veneficum

Abstract

Shewanella sp. IRI-160 is an algicidal bacterium that secretes an algicide, IRI-160AA. This algicide specifically targets dinoflagellates, while having no adverse effects on other algal species tested. Dinoflagellates exposed to IRI-160AA exhibited increased production of reactive oxygen species (ROS), DNA damage, and cell cycle arrest, implying a programmed pathway leading to cell death (PCD). Here, a metabolomic analysis was conducted on dinoflagellate Karlodinium veneficum and a control cryptophyte species Rhodomonas exposed to IRI-160AA to investigate the cellular mechanisms behind the physiological effects and the specificity of this algicide. Results of this research supported previous observations about physiological responses to the algicide. A suite of metabolites was identified that increased in the cell pellets of K. veneficum but not in Rhodomonas, including oxidative stress biomarkers, antioxidants, and compounds involved in DNA damage and PCD. Overall, the results of this study illustrated the metabolomic mechanisms underlying the algicidal effects of IRI-160AA on dinoflagellates. This research also provided insights and future directions for studies on the cellular response of dinoflagellates exposed to antagonistic bacteria in the environment.

Transcriptome profiling reveals a global response in harmful dinoflagellate Karlodinium veneficum to naturally-occurring bacterial algicides

“…Evidence for a global response to the algicide includes impacts on various biological processes at the transcriptional, post-transcriptional, and post-translational levels as supported by the transcriptome data. IRI-160AA stimulated ROS production, inducing the formation of biomarkers for oxidative stress, antioxidants, other compounds involved in DNA damage and programmed cell death, as well as the chlorophyll precursor in the cell pellets of the algicide treatment of K. veneficum (Wang and Coyne, 2022). Results also point to photoinactivation and accompanied photorepair in cells exposed to IRI-160AA.…”

“…Previous research indicated IRI-160AA induced ROS (specifically H 2 O 2 ) production, DNA damage, and cell cycle arrest, as well as other markers of PCD in dinoflagellates (Pokrzywinski et al, 2017b), accompanied by impaired photosynthetic efficiency and PSII inhibition (Tilney et al, 2014). Recent metabolomics analysis also demonstrated the enrichment of a suite of compounds in K. veneficum by the algicide IRI-160AA, including oxidative stress biomarkers, antioxidants, compounds involved in DNA damage and PCD, as well as the chlorophyll precursor 5-aminolevulinic acid (Figure 5) (Wang and Coyne, 2022). An intertwined relationship between these markers and PCD, as well as photosynthesis, has also been noted in plants (Yoshiyama et al, 2013;Mhamdi and Van Breusegem, 2018) and other algal species (Rezayian et al, 2019;Zhao et al, 2019;Zhao et al, 2020).…”

“…The pathway of phytochromobilin formation is not shown in detail (dashed arrow). The metabolite (5-aminolevulinic acid [ALA]) shown in blue increased in the cell pellets of Karlodinium veneficum treated with IRI-160AA (Wang and Coyne, 2022). DEGs identified in the algicide treatment of K. veneficum were indicated in red.…”

“…DEGs identified in the algicide treatment of K. veneficum were indicated in red. Besides the metabolite and genes, arrows indicate the increase or decrease of the content (of the metabolite) (Wang and Coyne, 2022) or expression (of genes) in K. veneficum treated with IRI-160AA compared to the control. The stimulatory effect of ALA on chlorophyll biosynthesis intermediates (Aarti et al, 2006;Stenbaek et al, 2008;Wu et al, 2018) was indicated by a grey arrow; the feedback inhibitory impact of these intermediates on ALA biosynthesis (Pattanayak and Tripathy, 2011) was indicated by a grey line with a bar.…”

“…DNA degradation, reactive oxygen species (ROS) production, as well as caspase 3-like protease (DEVDase) activity were also observed in these organisms, implying a programmed pathway leading to cell death (PCD) (Pokrzywinski et al, 2017b). Recent metabolomics research on K. veneficum treated with IRI-160AA demonstrated an increase of a suite of compounds in the cell pellets of this alga, including oxidative stress biomarkers, antioxidants, and compounds involved in DNA damage and PCD (Wang and Coyne, 2022).…”