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Common and Species-Specific Effects of Phosphate on Marine Microalgae Fatty Acids Shape Their Function in Phytoplankton Trophic Ecology

  • Environmental Microbiology
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Abstract

The use of fatty acids (FA) to infer structure of phytoplankton assemblages and as indicators of microalgae nutritional value is acquiring relevance in modern phytoplankton ecology and new advances concerning factors influencing FA variability among microalgae are demanded. In this regard, the relationship between phosphorus and FA remains particularly little studied in marine phytoplankton. In the present study, we focus on phosphate effects on FA from a diversified set of marine microalgae and provide new insights into the applicability of FA in phytoplankton trophic ecology. Phosphate deprivation mainly induced monounsaturated FA production in eight out of nine microalgae and their changes were species-specific, with palmitoleic acid exhibiting extreme variation and discriminating between haptophyte classes. The important phosphate-induced and interspecific variability found for oleic acid was perceived as a concern for the current application of this FA as a trophic position indicator in grazers. Chloroplast C-16 and C-18 polyunsaturated FA were more affected by phosphate than C-20 and C-22 highly unsaturated FA (HUFA). The relative stability of stearidonic acid to phosphate in cryptophytes and haptophytes pinpointed this FA as a suited marker for both microalgae groups. Taken all species together, phosphate deprivation and taxonomy accounted for 20.8 and 50.7% of total FA variation, respectively. HUFA were minimally affected by phosphate indicating their suitability as indicators of phytoplankton trophic value. The asymptotic relationship between HUFA and phosphorus cell content suggested mineral composition (phosphorus) could be more important than HUFA content as attribute of marine microalgae nutritional value at the species level.

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Acknowledgments

This research was supported by projects “Sustainable and environmentally friendly aquaculture for the Atlantic Region of Europe” (SEAFARE), funded by the European Union Atlantic Area 670 Transnational Programme (2007–2013) through grant no 2009-1/123 and EI.AVA.AVA201301.5 (New technologies for aquaculture enhancement and diversification in Andalusia).

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  1. IFAPA Centro El Toruño. Andalusia Research and Training Institute for Fisheries and Agriculture, 11500-El Puerto de Santa María, Cádiz, Spain

    José Pedro Cañavate, Isabel Armada & Ismael Hachero-Cruzado

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  1. José Pedro Cañavate
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  2. Isabel Armada
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  3. Ismael Hachero-Cruzado
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Correspondence to José Pedro Cañavate.

Electronic Supplementary Material

Fig. S1

Principal coordinate ordination of studied microalgae arranged according to taxonomy and phosphate nutrition stage of phosphate repletion (PR, solid symbols) and phosphate replenishment following phosphate depletion for 7 d (PDR, empty symbols) and using FA as descriptor variables. (GIF 99 kb)

High resolution image (TIFF 979 kb)

Fig. S2

Principal coordinate analysis for microalgae growth stages in the nine studied species using their fatty acids and main glycerolipids as descriptor variables under phosphate repletion for 3 d (PR-3) and 7 d (PR-7), phosphate depletion for 3 d (PD-3) and 7 d (PD-7), phosphate depletion following PD for 3 d (PDD-3) and 7 d (PDD-7), and phosphate replenishment after PD for 3 d (PDR-3) and 7 d (PDR-7). Glycerolipids included the following lipid classes: diacylglyceryl-N,N,N-trimethylhomoserine (DGTS), diacylglycerol hydroxymethyl-N,N,N-trimethyl-β-alanine (DGTA) and diacylglycerol-carboxyhydroxymethylcholine (DGCC), sulphoquinovosyl-diacylglicerol (SQDG), monogalactosyl-diacylglicerol (MGDG), digalactosyl-diacylglicerol (DGDG), phosphatidylcholine (PC), phosphatidylethanolamine (PE), phosphatidylglycerol (PG) and triglycerides (TG). (GIF 186 kb)

High resolution image (TIFF 3695 kb)

Fig. S3

Mean (±standard deviation) relative variation (%) from phosphate repletion (PR) to phosphate depletion for 14 d (PDD) and from PDD to phosphate replenishment (PDR) in saturated (SAFA), monounsaturated (MUFA) and polyunsaturated (PUFA) fatty acids. Same letters denote lack of significance (one-way ANOVA, p > 0.05) among microalgae species. (GIF 2023 kb)

High resolution image (TIFF 1095 kb)

Fig. S4

Mean (±standard deviation) relative variation (%) from phosphate repletion (PR) to phosphate depletion for 14 d (PDD) and from PDD to phosphate replenishment (PDR) in total n3 (n3), total n6 (n6) and the ratio between n3 and n6 (n3/n6) fatty acids. Same letters denote lack of significance (one-way ANOVA, p > 0.05) among microalgae species. (GIF 1481 kb)

High resolution image (TIFF 1160 kb)

Fig. S5

Mean (±standard deviation) content (mg fatty acid g−1 dw) in total C-16, C-18, C-20 and C-22 fatty acids in the studied microalgae under phosphate repletion (PR), phosphate depletion after 7 d (PR) and phosphate depletion after 14 d (PDD). Different letters denote significant differences (one-way ANOVA, p < 0.05) within each microalgae due to phosphate treatment. (GIF 2417 kb)

High resolution image (TIFF 1289 kb)

Fig. S6

Best fitting regression equation and 95% confidence interval of total highly unsaturated fatty acids (HUFA) against phosphorus cell quota in the nine studied microalgae. The proportion of total variance explained by the regression is indicated by r2. (GIF 125 kb)

High resolution image (TIFF 1295 kb)

Fig. S7

Best fitting regression equation and 95% confidence interval of total n3 fatty acids (n3) against phosphorus cell quota in the nine studied microalgae. The proportion of total variance explained by the regression is indicated by r2. (GIF 139 kb)

High resolution image (TIFF 1292 kb)

Fig. S8

Best fitting regression equation and 95% confidence interval of total n6 fatty acids (n6) against phosphorus cell quota in the nine studied microalgae. The proportion of total variance explained by the regression is indicated by r2. (GIF 133 kb)

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Table S1

Mean fatty acid content and standard deviation (SD), expressed as mg g−1 dw, of microalgae cultured in phosphate replete medium for 3 d (PR-3) and 7 d (PR-7), phosphate deplete medium for 3 d (PD-3), 7 d (PD-7), 10 d (PD-10) and 14 d (PD-14), and phosphate replenishment after PD-7 for 3 d (PDR-3) and 7 d (PDR-7). Hom denotes homogeneous phosphate groups (p < 0.05; Tukey pos hoc test; n = 6) after one-way ANOVA analysis. Probabilities (p) derived from the two-way ANOVA analysis are provided for each factor (P stage; Age) and their interaction (PxAge). (XLSX 111 kb)

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Cañavate, J.P., Armada, I. & Hachero-Cruzado, I. Common and Species-Specific Effects of Phosphate on Marine Microalgae Fatty Acids Shape Their Function in Phytoplankton Trophic Ecology. Microb Ecol 74, 623–639 (2017). https://doi.org/10.1007/s00248-017-0983-1

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