Dataset Information

Gene expression in the mixotrophic prymnesiophyte, Prymnesium parvum, responds to prey availability.

ABSTRACT: The mixotrophic prymnesiophyte, Prymnesium parvum, is a widely distributed alga with significant ecological importance. It produces toxins and can form ecosystem disruptive blooms that result in fish kills and changes in planktonic food web structure. However, the relationship between P. parvum and its prey on the molecular level is poorly understood. In this study, we used RNA-Seq technology to study changes in gene transcription of P. parvum in three treatments with different microbial populations available as potential prey: axenic P. parvum (no prey), bacterized P. paruvm, and axenic P. parvum with ciliates added as prey. Thousands of genes were differentially expressed among the three treatments. Most notably, transcriptome data indicated that P. parvum obtained organic carbon, including fatty acids, from both bacteria and ciliate prey for energy and cellular building blocks. The data also suggested that different prey provided P. parvum with macro- and micro-nutrients, namely organic nitrogen in the form of amino acids from ciliates, and iron from bacteria. However, both transcriptomic data and growth experiments indicated that P. parvum did not grow faster in the presence of prey despite the gains in nutrients, although algal abundances attained in culture were slightly greater in the presence of prey. The relationship between phototrophy, heterotrophy and growth of P. parvum is discussed.

SUBMITTER: Liu Z

PROVIDER: S-EPMC4403553 | biostudies-literature | 2015

REPOSITORIES: biostudies-literature

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Gene expression in the mixotrophic prymnesiophyte, Prymnesium parvum, responds to prey availability.

Liu Zhenfeng Z Jones Adriane C AC Campbell Victoria V Hambright K David KD Heidelberg Karla B KB Caron David A DA

Frontiers in microbiology 20150420

The mixotrophic prymnesiophyte, Prymnesium parvum, is a widely distributed alga with significant ecological importance. It produces toxins and can form ecosystem disruptive blooms that result in fish kills and changes in planktonic food web structure. However, the relationship between P. parvum and its prey on the molecular level is poorly understood. In this study, we used RNA-Seq technology to study changes in gene transcription of P. parvum in three treatments with different microbial populat ...[more]

PMID: 25941521

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Project description:BACKGROUND:Ochromonas is a genus of mixotrophic chrysophytes that is found ubiquitously in many aquatic environments. Species in this genus can be important consumers of bacteria but vary in their ability to perform photosynthesis. We studied the effect of light and bacteria on growth and gene expression of a predominantly phagotrophic Ochromonas species. Axenic cultures of Ochromonas sp. were fed with heat-killed bacteria (HKB) and grown in constant light or darkness. RNA was extracted from cultures in the light or in the dark with HKB present (Light?+?HKB; Dark?+?HKB), and in the light after HKB were depleted (Light?+?depleted HKB). RESULTS:There were no significant differences in the growth or bacterial ingestion rates between algae grown in light or dark conditions. The availability of light led to a differential expression of only 8% of genes in the transcriptome. A number of genes associated with photosynthesis, phagotrophy, and tetrapyrrole synthesis was upregulated in the Light?+?HKB treatment compared to Dark?+?HKB. Conversely, the comparison between the Light?+?HKB and Light?+?depleted HKB treatments revealed that the presence of HKB led to differential expression of 59% of genes, including the majority of genes involved in major carbon and nitrogen metabolic pathways. Genes coding for unidirectional enzymes for the utilization of glucose were upregulated in the presence of HKB, implying increased glycolytic activities during phagotrophy. Algae without HKB upregulated their expression of genes coding for ammonium transporters, implying uptake of inorganic nitrogen from the culture medium when prey were unavailable. CONCLUSIONS:Transcriptomic results agreed with previous observations that light had minimal effect on the population growth of Ochromonas sp. However, light led to the upregulation of a number of phototrophy- and phagotrophy-related genes, while the availability of bacterial prey led to prominent changes in major carbon and nitrogen metabolic pathways. Our study demonstrated the potential of transcriptomic approaches to improve our understanding of the trophic physiologies of complex mixotrophs, and revealed responses in Ochromonas sp. not apparent from traditional culture studies.

Project description:Mixotrophic flagellates, which have diverse nutritional modes and play important roles in connecting the microbial loop with the classical food chain, are ideal models to study the mechanisms of adaptation between different nutritional modes in protists. In their natural ecosystems, mixotrophic flagellates may encounter microalgal prey of different digestibility, which may affect the carbon flow. To date, a molecular biological view of the metabolic processes in the mixotrophic flagellate Poterioochromonas malhamensis during nutritional adaptation and feeding on microalgal prey of different digestibility is still lacking. Accordingly, this study focused on the gene expression differences in P. malhamensis under autotrophy, being fed by the digestible microalga Chlorella sorokiniana GT-1, and being fed by the indigestible microalga C. sorokiniana CMBB-146. Results showed that the growth rate of P. malhamensis under autotrophy was much lower than that when fed by digestible microalgae. Addition of C. sorokiniana CMBB-146 could only increase the growth rate of P. malhamensis in the first 3 days, but the cell concentration of P. malhamensis started to decrease gradually after 4 days. Compared to autotrophic P. malhamensis, total 6,583 and 3,510 genes were significantly and differentially expressed in P. malhamensis fed by digestible microalgae and indigestible microalgae, respectively. Compared to autotrophic cells, genes related to the ribosome, lysosome, glycolysis, gluconeogenesis, TCA cycle, β-oxidation, duplication, and β-1,3-glucan in P. malhamensis grazing on digestible prey were up-regulated, while genes related to light harvesting and key enzymes referring to chlorophyll were down-regulated. Genes related to apoptosis and necrosis in P. malhamensis were up-regulated after grazing on indigestible microalgae compared to the autotrophic group, which we suggest is associated with the up-regulation of genes related to lysosome enzymes. This study provides abundant information on the potential intracellular physiological responses of P. malhamensis during the process of nutritional adaptation.

Dataset Information

Gene expression in the mixotrophic prymnesiophyte, Prymnesium parvum, responds to prey availability.

Publications

Gene expression in the mixotrophic prymnesiophyte, Prymnesium parvum, responds to prey availability.

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