Ecological and evolutionary processes involved in shaping microbial habitat generalists and specialists in urban park ecosystems

Author:

Li Shuzhen1ORCID,Yan Xue12,Abdullah Al Mamun1,Ren Kexin1,Rensing Christopher13,Hu Anyi4ORCID,Tsyganov Andrey N.5,Mazei Yuri567,Smirnov Alexey8,Mazei Natalia5,Yang Jun1ORCID

Affiliation:

1. Aquatic EcoHealth Group, Fujian Key Laboratory of Watershed Ecology, Key Laboratory of Urban Environment and Health, Institute of Urban Environment, Chinese Academy of Sciences, Xiamen, China

2. University of Chinese Academy of Sciences, Beijing, China

3. Institute of Environmental Microbiology, College of Resources and the Environment, Fujian Agriculture & Forestry University, Fuzhou, China

4. CAS Key Laboratory of Urban Pollutant Conversion, Institute of Urban Environment, Chinese Academy of Sciences, Xiamen, China

5. Lomonosov Moscow State University, Moscow, Russia

6. Faculty of Biology, Shenzhen MSU-BIT University, Shenzhen, China

7. A.N. Severtsov Institute of Ecology and Evolution, Russian Academy of Sciences, Moscow, Russia

8. Department of Invertebrate Zoology, Faculty of Biolog, St. Petersburg University, St Petersburg, Russia

Abstract

ABSTRACT Microbiomes are integral to ecological health and human well-being; however, their ecological and evolutionary drivers have not been systematically investigated, especially in urban park ecosystems. As microbes have different levels of tolerance to environmental changes and habitat preferences, they can be categorized into habitat generalists and specialists. Here, we explored the ecological and evolutionary characteristics of both prokaryotic and microeukaryotic habitat generalists and specialists from six urban parks across five habitat types, including moss, soil, tree hole, water, and sediment. Our results revealed that different ecological and evolutionary processes maintained and regulated microbial diversity in urban park ecosystems. Under ecological perspective, community assembly of microbial communities was mainly driven by stochastic processes; however, deterministic processes were higher for habitat specialists than generalists. Microbial interactions were highly dynamic among habitats, and habitat specialists played key roles as module hubs in intradomain networks. In aquatic interdomain networks, microeukaryotic habitat specialists and prokaryotic habitat specialists played crucial roles as module hubs and connectors, respectively. Furthermore, analyzing evolutionary characteristics, our results revealed that habitat specialists had a much higher diversification potential than generalists, while generalists showed shorter phylogenetic branch lengths as well as larger genomes than specialists. This study broadens our understanding of the ecological and evolutionary features of microbial habitat generalists and specialists in urban park ecosystems across multi-habitat. IMPORTANCE Urban parks, as an important urban greenspace, play essential roles in ecosystem services and are important hotspots for microbes. Microbial diversity is driven by different ecological and evolutionary processes, while little is currently known about the distinct roles of ecological and evolutionary features in shaping microbial diversity in urban park ecosystems. We explored the ecological and evolutionary characteristics of prokaryotic and microeukaryotic habitat generalists and specialists in urban park ecosystems based on a representative set of different habitats. We found that different ecological and evolutionary drivers jointly maintained and regulated microbial diversity in urban park microbiomes through analyzing the community assembly process, ecological roles in hierarchical interaction, and species diversification potential. These findings significantly advance our understanding regarding the mechanisms governing microbial diversity in urban park ecosystems.

Funder

National Natural Science Foundation of China

"Fujian STS" Program of the Chinese Academy of Sciences

Russian Science Foundation

Publisher

American Society for Microbiology

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