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Genome-wide transcriptome analysis revealed organelle specific responses to temperature variations in algae

View Article: PubMed Central - PubMed

ABSTRACT

Temperature is a critical environmental factor that affects microalgal growth. However, microalgal coping mechanisms for temperature variations are unclear. Here, we determined changes in transcriptome, total carbohydrate, total fatty acid methyl ester, and fatty acid composition of Tetraselmis sp. KCTC12432BP, a strain with a broad temperature tolerance range, to elucidate the tolerance mechanisms in response to large temperature variations. Owing to unavailability of genome sequence information, de novo transcriptome assembly coupled with BLAST analysis was performed using strand specific RNA-seq data. This resulted in 26,245 protein-coding transcripts, of which 83.7% could be annotated to putative functions. We identified more than 681 genes differentially expressed, suggesting an organelle-specific response to temperature variation. Among these, the genes related to the photosynthetic electron transfer chain, which are localized in the plastid thylakoid membrane, were upregulated at low temperature. However, the transcripts related to the electron transport chain and biosynthesis of phosphatidylethanolamine localized in mitochondria were upregulated at high temperature. These results show that the low energy uptake by repressed photosynthesis under low and high temperature conditions is compensated by different mechanisms, including photosystem I and mitochondrial oxidative phosphorylation, respectively. This study illustrates that microalgae tolerate different temperature conditions through organelle specific mechanisms.

No MeSH data available.


The reconstructed lipid biosynthesis pathway of Tetraselmis sp. KCTC12432BP.The green arrows indicate reactions that occur only in the plastid and the black arrow indicate reactions that may occur in different cell parts. The enzymes are represented by a light blue circle with grey labels, and substrate/product is represented by white circles with black labels. The colour index indicates the expression pattern of the enzymes in low mid and high temperatures. Abbreviations: DAG, diacylglycerol; DHAP, dihydroxyacetone phosphate; GAPDH, glyceraldehyde-3-phosphate dehydrogenase; G3P, glycerol 3-phosphate; GPAT, glycerol-3-phosphate acyltransferase; LPA, lysophosphatidic acid; LPAAT, lysophosphatidic acid acyltransferase; MS, monogalactosyldiacylglycerol synthase; PA, phosphatidic acid; PAP, phosphatidate phosphatase; PE, phosphatidylethanolamine; PG, phosphatidylglycerol; PGP-P, phosphatidylglycerol-phosphate; PGP1, phosphatidylglycerolphosphate synthase; PGPA, phosphatidylglycerolphosphatase A; PSS, phosphtidylserine synthase; PSD, phosphatidylserine decarboxylase; Ptd-l-Ser, phosphatidylserine.
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f3: The reconstructed lipid biosynthesis pathway of Tetraselmis sp. KCTC12432BP.The green arrows indicate reactions that occur only in the plastid and the black arrow indicate reactions that may occur in different cell parts. The enzymes are represented by a light blue circle with grey labels, and substrate/product is represented by white circles with black labels. The colour index indicates the expression pattern of the enzymes in low mid and high temperatures. Abbreviations: DAG, diacylglycerol; DHAP, dihydroxyacetone phosphate; GAPDH, glyceraldehyde-3-phosphate dehydrogenase; G3P, glycerol 3-phosphate; GPAT, glycerol-3-phosphate acyltransferase; LPA, lysophosphatidic acid; LPAAT, lysophosphatidic acid acyltransferase; MS, monogalactosyldiacylglycerol synthase; PA, phosphatidic acid; PAP, phosphatidate phosphatase; PE, phosphatidylethanolamine; PG, phosphatidylglycerol; PGP-P, phosphatidylglycerol-phosphate; PGP1, phosphatidylglycerolphosphate synthase; PGPA, phosphatidylglycerolphosphatase A; PSS, phosphtidylserine synthase; PSD, phosphatidylserine decarboxylase; Ptd-l-Ser, phosphatidylserine.

Mentions: To verify the organelle level changes under different temperature conditions, we next investigated if genes responsible for lipid structure are also differentially expressed. Since the lipid structure plays an important role in cellular metabolism and many of the differentially expressed genes were localized specifically in the thylakoid and mitochondrial membranes, we reconstructed the lipid pathway from the transcriptome assembly and analysed their expression patterns (Fig. 3). Glycerol-3-phosphate acyltransferase, which encodes the enzyme that converts glycerol 3-phosphate to lysophosphatidic acid (LPA), increased in the low-temperature conditions (TR233525_c1_g1). Furthermore, GO annotation for TR233525_c1_g1 showed that this protein was localized in the plastid, which indicated the increased LPA level in the plastid. As LPA synthesis is a rate-limiting reaction step of lipid biosynthesis in the plastid, this data suggests increased levels of galactoglycerolipids, such as MGDG and DGDG, and phosphoglycerolipids, such as PG, from the plastidic pathway34. However, enzymes responsible for synthesis of PE were upregulated in high-temperature conditions (Fig. 3). Since PE is the main lipid structure that composes the inner membrane of mitochondria along with phosphatidylcholine, this data suggests further proof for activation of mitochondrial energy uptake processes being activated in high-temperature conditions3536.


Genome-wide transcriptome analysis revealed organelle specific responses to temperature variations in algae
The reconstructed lipid biosynthesis pathway of Tetraselmis sp. KCTC12432BP.The green arrows indicate reactions that occur only in the plastid and the black arrow indicate reactions that may occur in different cell parts. The enzymes are represented by a light blue circle with grey labels, and substrate/product is represented by white circles with black labels. The colour index indicates the expression pattern of the enzymes in low mid and high temperatures. Abbreviations: DAG, diacylglycerol; DHAP, dihydroxyacetone phosphate; GAPDH, glyceraldehyde-3-phosphate dehydrogenase; G3P, glycerol 3-phosphate; GPAT, glycerol-3-phosphate acyltransferase; LPA, lysophosphatidic acid; LPAAT, lysophosphatidic acid acyltransferase; MS, monogalactosyldiacylglycerol synthase; PA, phosphatidic acid; PAP, phosphatidate phosphatase; PE, phosphatidylethanolamine; PG, phosphatidylglycerol; PGP-P, phosphatidylglycerol-phosphate; PGP1, phosphatidylglycerolphosphate synthase; PGPA, phosphatidylglycerolphosphatase A; PSS, phosphtidylserine synthase; PSD, phosphatidylserine decarboxylase; Ptd-l-Ser, phosphatidylserine.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC5121895&req=5

f3: The reconstructed lipid biosynthesis pathway of Tetraselmis sp. KCTC12432BP.The green arrows indicate reactions that occur only in the plastid and the black arrow indicate reactions that may occur in different cell parts. The enzymes are represented by a light blue circle with grey labels, and substrate/product is represented by white circles with black labels. The colour index indicates the expression pattern of the enzymes in low mid and high temperatures. Abbreviations: DAG, diacylglycerol; DHAP, dihydroxyacetone phosphate; GAPDH, glyceraldehyde-3-phosphate dehydrogenase; G3P, glycerol 3-phosphate; GPAT, glycerol-3-phosphate acyltransferase; LPA, lysophosphatidic acid; LPAAT, lysophosphatidic acid acyltransferase; MS, monogalactosyldiacylglycerol synthase; PA, phosphatidic acid; PAP, phosphatidate phosphatase; PE, phosphatidylethanolamine; PG, phosphatidylglycerol; PGP-P, phosphatidylglycerol-phosphate; PGP1, phosphatidylglycerolphosphate synthase; PGPA, phosphatidylglycerolphosphatase A; PSS, phosphtidylserine synthase; PSD, phosphatidylserine decarboxylase; Ptd-l-Ser, phosphatidylserine.
Mentions: To verify the organelle level changes under different temperature conditions, we next investigated if genes responsible for lipid structure are also differentially expressed. Since the lipid structure plays an important role in cellular metabolism and many of the differentially expressed genes were localized specifically in the thylakoid and mitochondrial membranes, we reconstructed the lipid pathway from the transcriptome assembly and analysed their expression patterns (Fig. 3). Glycerol-3-phosphate acyltransferase, which encodes the enzyme that converts glycerol 3-phosphate to lysophosphatidic acid (LPA), increased in the low-temperature conditions (TR233525_c1_g1). Furthermore, GO annotation for TR233525_c1_g1 showed that this protein was localized in the plastid, which indicated the increased LPA level in the plastid. As LPA synthesis is a rate-limiting reaction step of lipid biosynthesis in the plastid, this data suggests increased levels of galactoglycerolipids, such as MGDG and DGDG, and phosphoglycerolipids, such as PG, from the plastidic pathway34. However, enzymes responsible for synthesis of PE were upregulated in high-temperature conditions (Fig. 3). Since PE is the main lipid structure that composes the inner membrane of mitochondria along with phosphatidylcholine, this data suggests further proof for activation of mitochondrial energy uptake processes being activated in high-temperature conditions3536.

View Article: PubMed Central - PubMed

ABSTRACT

Temperature is a critical environmental factor that affects microalgal growth. However, microalgal coping mechanisms for temperature variations are unclear. Here, we determined changes in transcriptome, total carbohydrate, total fatty acid methyl ester, and fatty acid composition of Tetraselmis sp. KCTC12432BP, a strain with a broad temperature tolerance range, to elucidate the tolerance mechanisms in response to large temperature variations. Owing to unavailability of genome sequence information, de novo transcriptome assembly coupled with BLAST analysis was performed using strand specific RNA-seq data. This resulted in 26,245 protein-coding transcripts, of which 83.7% could be annotated to putative functions. We identified more than 681 genes differentially expressed, suggesting an organelle-specific response to temperature variation. Among these, the genes related to the photosynthetic electron transfer chain, which are localized in the plastid thylakoid membrane, were upregulated at low temperature. However, the transcripts related to the electron transport chain and biosynthesis of phosphatidylethanolamine localized in mitochondria were upregulated at high temperature. These results show that the low energy uptake by repressed photosynthesis under low and high temperature conditions is compensated by different mechanisms, including photosystem I and mitochondrial oxidative phosphorylation, respectively. This study illustrates that microalgae tolerate different temperature conditions through organelle specific mechanisms.

No MeSH data available.