Warming degrades nutritional quality of periphyton in stream ecosystems: evidence from a mesocosm experiment

Abstract

Periphyton, which is rich in polyunsaturated fatty acids (PUFA), serves as an indispensable high-quality basal resource for consumers in stream food webs. However, with global warming, how fatty acid composition of periphyton changes and consequent effects on their transfer to higher trophic level consumers remain unclear. By carrying out a manipulative mesocosm experiment with a 4°C increase, warming led to a significant decrease in the proportions of PUFA and Long-chain PUFA (LC-PUFA, >20 C) in periphyton from 13.32% to 9.90% and from 3.05% to 2.18%, respectively. The proportions of three PUFAs-α-linolenic acid (18:3ω3), arachidonic acid (ARA, 20:4ω6), and docosahexaenoic acid (22:6ω3)-also declined significantly (P < .05). Notably, the fatty acid profile of the consumer-Bellamya aeruginosa reflected the changes in basal resources, with a decrease in PUFA from 40.14% to 36.27%, and a significant decrease in LC-PUFA from 34.58% to 30.11%. Although algal community composition in biofilms did not significantly change with warming, significant transcriptomic alterations were observed, with most differentially expressed genes related to fatty acid synthesis in lipid metabolism and photosynthesis down-regulated. Our findings indicate that warming may hinder the production and transfer of high-quality carbon evaluated by LC-PUFA to consumers, consequently affect the complexity and stability of stream food webs.

Keywords: fatty acid; food quality; nutrient transfer; periphyton; river ecosystem; transcriptome; warming.

Figure 1

Mesocosm experiment setup (A, B), including sampling of water and cobbles with periphyton (also called epilithic biofilms) from their original habitat (C). The facility consisted of 10 fully flow-through mesocosms (volume: 1000 L; diameter: 1.2 m; height: 0.8 m). Each set of mesocosms was filled with water and supplemented with cobbles and consumers (Bellamya aeruginosa).

Figure 2

The NMDS analysis of fatty acid composition in periphyton on rocks (A) and Bellamya aeruginosa (B). A, ambient; W, warmed; T, initially. Stress <0.2 indicates that the model fits well.

Figure 3

Changes in the proportion (percentages of the total fatty acids, mean ± SE, n = 5) of fatty acids in periphyton (A, C) and snails (B, D). SAFA, saturated fatty acids (fatty acids without double bonds); MUFA, monounsaturated fatty acids(fatty acids with one double bond); PUFA, polyunsaturated fatty acids (fatty acids with at least two double bonds, including ω3-PUFA and ω6-PUFA); LC-PUFA, a subclass of long-chain (≥ 20 C) PUFAs that contain more than 2 double bonds; ω3-PUFA, PUFA with the first double bond on the third carbon atom from the terminal methyl group; ω6-PUFA, PUFA with the first double bond on the sixth carbon atom from the terminal methyl group; LIN, linoleic acid (18:2ω6); ALA, α-linolenic acid (18:3ω3); ARA, arachidonic acid (20:4ω6); EPA, eicosapentaenoic acid (20:5ω3); DHA, docosahexaenoic acid (22:6ω3). (^*P < .05, ^**  P < .01).

Figure 4

Changes in density (A) and relative abundance (B) of algal communities in periphyton at the end of the experiment (mean ± SE, n = 5). Ambient: normal water temperature; warmed: increased by 4°C.

Figure 5

Quantity statistics bar chart (A) and volcano plot (B) of DEGs. In A, the vertical axis represents DEGs numbers, red represents the number of up-regulated DEGs (Warmed vs Ambient), and blue represents the number of down-regulated DEGs. In B, the horizontal axis indicates expression changes (log) of the genes in different treatments and the vertical axis shows the differences of gene expression. Splashes represent different genes. Gray dots are genes with no significant discrepancy, red dots are genes with significant upregulation, and blue dots are genes with significant downregulation.

Figure 6

Lipid metabolism (A), carbohydrate metabolism and energy metabolism (B) enrichment analysis of DEGs. The vertical axis indicates KEGG pathway and the horizontal axis represents the rich factor. The size of bubbles indicates the number of genes in the KEGG pathway. Pathways that are significantly upregulated (red bubbles) and significantly downregulated (green bubbles). (^* down-regulated P < .05).

Figure 7

Responses of several key metabolic pathways in periphyton to warming. (A) Fatty acid biosynthesis; (B) biosynthesis of unsaturated fatty acids; (C) photosynthesis. Significantly upregulated genes (red) and downregulated genes (blue) are displayed. For abbreviations of genes names, see Table S4. The bar chart represents the changes in differentially expressed genes over a period of 5 weeks, with the vertical axis indicating the mean log₂ (fold change) (warming vs ambient), and the error bars representing the SE (n = 3). SA (18:0), stearic acid; LIN, linoleic acid (18:2ω6); ALA, α-linolenic acid (18:3ω3); GLA (18:3ω6), γ-linolenic acid; ARA (20:4ω6), arachidonic acid; EPA (20:5ω3), eicosapentaenoic acid; DPA (22:5ω3), docosapentaenoic acid; DHA (22:6ω3), docosahexaenoic acid; PSI, photosystem I; PSII, photosystem II.