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Food quality upgrade of carbon from submerged macrophytes by flagellates via a heterotrophic pathway can stimulate growth of Daphnia magna

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Abstract

Submerged macrophytes play crucial roles in maintaining the stability of clear-water states in shallow lakes. Recent stable isotope studies have shown that crustacean zooplankton can utilize submerged macrophyte carbon, but macrophytes alone cannot support the growth and reproduction of such grazers, being deficient in highly unsaturated fatty acids (HUFA). We hypothesized that flagellates feeding on macrophytes can synthesize HUFA and thereby support crustacean zooplankton. To test this hypothesis, we conducted a feeding experiment in which Daphnia magna were provided with a diet of submerged macrophyte Hydrilla verticillata detritus which had been degraded by lake microbes. The chlorophyte Scenedesmus bijuga and undegraded macrophyte detritus were used as controls for comparison of Daphnia’s performance. Using biochemical analysis, we examined how the degradation process affected the food quality of the macrophyte. Flagellates were subsequently isolated from the degraded macrophyte and cultured heterotrophically to detect their HUFA synthesis. The 5-day degraded H. verticillata showed significantly higher HUFA concentrations than undegraded macrophyte detritus. They supported better Daphnia performance than undegraded macrophyte, being comparable with S. bijuga. Two isolated flagellates (SL-1 and SL-2), identified as Ochromonas sp. and Poterioochromonas sp., were found to contain HUFA when cultured heterotrophically without dietary sources of fatty acids, suggesting their HUFA synthesis ability. Our results demonstrate that submerged macrophytes may thus indirectly support crustacean zooplankton via flagellate mediation. As crustacean zooplanktons are of key importance for water quality in the grazer control of phytoplankton, this microbial facilitation may contribute to the maintenance of macrophyte clear-water conditions in shallow lakes.

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Availability of data and material

The sequence data have been submitted to the GenBank databases under accession number OP420791 and OP420792. Other data generated or analyzed during this study are included in this article.

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Acknowledgements

We are grateful for the work of numerous participants who collected and analyzed samples during the experimental period. We thank Anne Mette Poulsen and Amy-Jane Beer for English editing.

Funding

This study was funded by the National Natural Science Foundation of China (No. 32071566, 32211530454) and Natural Science Foundation of Guangdong Province (No. 2022A1515011074). EJ was supported by the TÜBITAK program BIDEB2232 (Project 118C250).

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Contributions

YT, ZL and LS conceived and designed the experiments. LS, S Liang, S Liu, YT and ZL performed the experiments. YT, LS, ZL and EJ analyzed the data. YT and LS wrote the manuscript. ZL and EJ revised it critically for important intellectual content; other authors provided editorial advice.

Corresponding authors

Correspondence to Yali Tang or Zhengwen Liu.

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We declare no conflict of interest/competing interests.

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This article does not contain any studies with human participants or animals performed by any of the authors.

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Additional information

Communicated by Maarten Boersma.

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Supplementary file1 (DOCX 94 KB)

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Tang, Y., Su, L., Liang, S. et al. Food quality upgrade of carbon from submerged macrophytes by flagellates via a heterotrophic pathway can stimulate growth of Daphnia magna. Oecologia 203, 467–476 (2023). https://doi.org/10.1007/s00442-023-05479-7

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  • DOI: https://doi.org/10.1007/s00442-023-05479-7

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