Prokaryotic and eukaryotic periphyton responses to warming, nutrient enrichment and small omnivorous fish: a shallow lake mesocosms experiment

Han Yang; Yu Cao; Wei Zhang; Juan Pablo Pacheco; Tong Liu; Yaqi Zheng; Erik Jeppesen; Liqing Wang

doi:10.1016/j.envres.2025.120942

Prokaryotic and eukaryotic periphyton responses to warming, nutrient enrichment and small omnivorous fish: a shallow lake mesocosms experiment

Environ Res. 2025 Jan 25:120942. doi: 10.1016/j.envres.2025.120942. Online ahead of print.

Authors

Han Yang¹, Yu Cao², Wei Zhang³, Juan Pablo Pacheco⁴, Tong Liu¹, Yaqi Zheng¹, Erik Jeppesen⁵, Liqing Wang⁶

Affiliations

¹ Key laboratory of Exploration and Utilization of Aquatic Genetic Resources of the Ministry of Education, Engineering Research Center of Environmental DNA and Ecological Water Health Assessment, Shanghai Ocean University, Shanghai 201306, China.
² Research Center of Aquatic Plant, Wuhan Botanical Garden, Chinese Academy of Sciences, Wuhan 430074, China.
³ Key laboratory of Exploration and Utilization of Aquatic Genetic Resources of the Ministry of Education, Engineering Research Center of Environmental DNA and Ecological Water Health Assessment, Shanghai Ocean University, Shanghai 201306, China. Electronic address: weizhang@shou.edu.cn.
⁴ Department of Ecology and Environmental Management, CURE - University of the Republic, Maldonado 20000, Uruguay; Department of Ecoscience, Aarhus University, Aarhus 8000, Denmark.
⁵ Department of Ecoscience, Aarhus University, Aarhus 8000, Denmark; Sino-Danish Centre for Education and Research (SDC), University of Chinese Academy of Sciences, Beijing 100049, China; Limnology Laboratory and EKOSAM, Department of Biological Sciences, Middle East Technical University, Ankara 06800, Turkey; Institute for Ecological Research and Pollution Control of Plateau Lakes, School of Ecology and Environmental Science, Yunnan University, Kunming, China.
⁶ Key laboratory of Exploration and Utilization of Aquatic Genetic Resources of the Ministry of Education, Engineering Research Center of Environmental DNA and Ecological Water Health Assessment, Shanghai Ocean University, Shanghai 201306, China. Electronic address: lqwang@shou.edu.cn.

PMID: 39870344
DOI: 10.1016/j.envres.2025.120942

Abstract

Global change stressors, including climate warming, eutrophication, and small-sized omnivorous fish, may exert interactive effects on the food webs and functioning of shallow lakes. Periphyton plays a central role in the primary production and nutrient cycling of shallow lakes but constitutes a complex community composed of eukaryotes and prokaryotes that may exhibit different responses to multiple environmental stressors with implications for the projections of the effects of global change on shallow lakes. We analyzed the effects of warming, nutrient enrichment, small omnivorous fish and their interactions on eukaryotic and prokaryotic periphyton structures in shallow lake mesocosms. We performed 16S and 18S rRNA high-throughput sequencing to elucidate the effect of the abovementioned stressors. We found that warming promoted periphytic alpha diversity and network complexity, with multi-tolerant genera becoming dominating (e.g. Spirosomaceae and Azospirillaceae). Contrastingly, nutrient enrichment led to reduced prokaryotic diversity and network complexity and stability, with weak disruption of the eukaryotic structure. Small omnivorous fish were major drivers of changes eukaryotic periphyton, facilitating diversity and network complexity, and increasing prokaryotic and eukaryotic biomarker diversity. Omnivorous fish reduced the grazing pressure on periphyton mainly through selective grazing on zooplankton, contributing to periphytic structural stability and functional diversity, especially the proliferation of prokaryotic biomarkers. Nutrient enrichment counteracted the positive effects of warming on periphyton, while concerted action with omnivorous fish led to high TN and TP concentrations and accelerated the negative development of periphytic alpha diversity and network structure. The co-occurrence of the three environmental pressures ultimately resulted in a disruption of periphytic biodiversity and community structure and weakened connectivity with the environment. Our study provided new insights into the understanding of the response of prokaryotic and eukaryotic community structure and ecological functions of freshwater periphyton to global environmental change.

Keywords: climate warming; global change; multiple stressors; nutrient enrichment; rRNA sequencing; small omnivorous fish.