Transcriptomic response of the toxic prymnesiophyte Prymnesium parvum (N. Carter) to phosphorus and nitrogen starvation

Beszteri, Sára; Yang, Ines; Jaeckisch, Nina; Tillmann, Urban; Frickenhaus, Stephan; Glöckner, Gernot; Cembella, Allan; John, Uwe

doi:10.1016/j.hal.2012.03.003

Cited by 34 publications

(28 citation statements)

References 71 publications

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“…Transcription of this family of transporters has been found to increase under P stress in the haptophyte, P. parvum (Beszteri et al, 2012), decrease when grown on urea vs. nitrate in cells of an unidentified cryptophyte (Terrado et al, 2015), and increase under N limitation for the pelagophyte, Aureococcus anophagefferens (Berg et al, 2008). This variable response across taxa is likely reflective of available nitrite levels within the cell rather than external concentrations (Galván, 2002; Maeda et al, 2014).…”

Section: Resultsmentioning

confidence: 99%

Conserved Transcriptional Responses to Nutrient Stress in Bloom-Forming Algae

et al. 2017

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The concentration and composition of bioavailable nitrogen (N) and phosphorus (P) in the upper ocean shape eukaryotic phytoplankton communities and influence their physiological responses. Phytoplankton are known to exhibit similar physiological responses to limiting N and P conditions such as decreased growth rates, chlorosis, and increased assimilation of N and P. Are these responses similar at the molecular level across multiple species? To interrogate this question, five species from biogeochemically important, bloom-forming taxa (Bacillariophyta, Dinophyta, and Haptophyta) were grown under similar low N, low P, and replete nutrient conditions to identify transcriptional patterns and associated changes in biochemical pools related to N and P stress. Metabolic profiles, revealed through the transcriptomes of these taxa, clustered together based on species rather than nutrient stressor, suggesting that the global metabolic response to nutrient stresses was largely, but not exclusively, species-specific. Nutrient stress led to few transcriptional changes in the two dinoflagellates, consistent with other research. An orthologous group analysis examined functionally conserved (i.e., similarly changed) responses to nutrient stress and therefore focused on the diatom and haptophytes. Most conserved ortholog changes were specific to a single nutrient treatment, but a small number of orthologs were similarly changed under both N and P stress in 2 or more species. Many of these orthologs were related to photosynthesis and may represent generalized stress responses. A greater number of orthologs were conserved across more than one species under low P compared to low N. Screening the conserved orthologs for functions related to N and P metabolism revealed increased relative abundance of orthologs for nitrate, nitrite, ammonium, and amino acid transporters under N stress, and increased relative abundance of orthologs related to acquisition of inorganic and organic P substrates under P stress. Although the global transcriptional responses were dominated by species-specific changes, the analysis of conserved responses revealed functional similarities in resource acquisition pathways among different phytoplankton taxa. This overlap in nutrient stress responses observed among species may be useful for tracking the physiological ecology of phytoplankton field populations.

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Section: Resultsmentioning

confidence: 99%

Conserved Transcriptional Responses to Nutrient Stress in Bloom-Forming Algae

et al. 2017

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“…) and Prymnesium parvum (Beszteri et al. ). In gram‐negative and gram‐positive bacteria, archaea, and eukaryotes, phosphate permeases are H + or Na + symporters.…”

Section: Cellular Pi Uptake and Assimilationmentioning

confidence: 99%

“…Clathrin‐mediated endocytosis proteins and autophagy‐related proteins were up‐regulated under Pi limitation in the dinoflagellate K. mikimotoi (Lei and Lu ), the haptophyte Prymnesium parvum (Beszteri et al. ), and the pelagophyte A. anophagefferens (Wurch et al. ).…”

Section: Adaptation and Acclimation Responses To Low‐p Stressmentioning

confidence: 99%

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Phosphorus physiological ecology and molecular mechanisms in marine phytoplankton

Lin

Litaker

Sunda

2016

Journal of Phycology

299

269

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Phosphorus (P) is an essential nutrient for marine phytoplankton and indeed all life forms. Current data show that P availability is growth-limiting in certain marine systems and can impact algal species composition. Available P occurs in marine waters as dissolved inorganic phosphate (primarily orthophosphate [Pi]) or as a myriad of dissolved organic phosphorus (DOP) compounds. Despite numerous studies on P physiology and ecology and increasing research on genomics in marine phytoplankton, there have been few attempts to synthesize information from these different disciplines. This paper is aimed to integrate the physiological and molecular information on the acquisition, utilization, and storage of P in marine phytoplankton and the strategies used by these organisms to acclimate and adapt to variations in P availability. Where applicable, we attempt to identify gaps in our current knowledge that warrant further research and examine possible metabolic pathways that might occur in phytoplankton from well-studied bacterial models. Physical and chemical limitations governing cellular P uptake are explored along with physiological and molecular mechanisms to adapt and acclimate to temporally and spatially varying P nutrient regimes. Topics covered include cellular Pi uptake and feedback regulation of uptake systems, enzymatic utilization of DOP, P acquisition by phagotrophy, P-limitation of phytoplankton growth in oceanic and coastal waters, and the role of P-limitation in regulating cell size and toxin levels in phytoplankton. Finally, we examine the role of P and other nutrients in the transition of phytoplankton communities from early succession species (diatoms) to late succession ones (e.g., dinoflagellates and haptophytes).

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“…In the laboratory, P. parvum tends to have higher toxicity when grown in N-or P-deficient conditions, i.e., unbalanced N∶P (Granéli et al 2012). Ambient environmental conditions during blooms of P. parvum generally corroborate these findings of stress-induced toxicity, i.e., blooms tend to occur under low N∶P availability (Aure and Rey 1992, Bales et al 1993, and researchers have hypothesized that the evolutionary benefit of toxigenesis is likely to be related to nutrient acquisition (Lewis 1986, Beszteri et al 2012, Remmel and Hambright 2012, Driscoll et al 2013). The need for nutrient acquisition would generally signal unfavorable, hence stressful, conditions for growth.…”

mentioning

confidence: 91%

Regulation of growth and toxicity of a mixotrophic microbe: implications for understanding range expansion in Prymnesium parvum

et al. 2014

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The rapid range expansion of the toxigenic marine haptophytic alga Prymnesium parvum in inland aquatic systems across the southern USA and beyond has prompted great interest in the ecology and evolutionary biology of this invasive bloom-forming species. Researchers have speculated that increased toxicity and heterotrophy in suboptimal environments allow blooms to develop in these new inland habitats that seem to represent extremes relative to P. parvum's perceived optimal niche. We used a laboratory-based study to elucidate the roles of salinity and nutrient availabilities in P. parvum growth and toxicity under environmental conditions representative of hypereutrophic reservoirs of the southwestern USA in which P. parvum blooms are now common. We found evidence that nutrient conditions favoring toxigenesis in P. parvum are suboptimal for growth and bloom formation, whereas conditions conducive to high growth rates are less favorable for toxigenesis. In contrast, both growth and toxicity scaled positively with salinity. Taken in the context of the documented biogeography of P. parvum and that toxigenesis in P. parvum probably evolved in support of heterotrophic nutrient acquisition, our results suggest that P. parvum's apparent range expansion into and across the USA is driven by increasing availabilities of salty and nutrient-rich systems, rather than by its toxigenic abilities.

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Transcriptomic response of the toxic prymnesiophyte Prymnesium parvum (N. Carter) to phosphorus and nitrogen starvation

Cited by 34 publications

References 71 publications

Conserved Transcriptional Responses to Nutrient Stress in Bloom-Forming Algae

Conserved Transcriptional Responses to Nutrient Stress in Bloom-Forming Algae

Phosphorus physiological ecology and molecular mechanisms in marine phytoplankton

Regulation of growth and toxicity of a mixotrophic microbe: implications for understanding range expansion in Prymnesium parvum

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