Gut microbial communities and their potential roles in cellulose digestion and thermal adaptation of earthworms

Yurong Yang; Mac A Callaham Jr; Xuefeng Wu; Yufeng Zhang; Donghui Wu; Deli Wang

doi:10.1016/j.scitotenv.2023.166666

Gut microbial communities and their potential roles in cellulose digestion and thermal adaptation of earthworms

Sci Total Environ. 2023 Dec 10:903:166666. doi: 10.1016/j.scitotenv.2023.166666. Epub 2023 Aug 31.

Authors

Yurong Yang¹, Mac A Callaham Jr², Xuefeng Wu¹, Yufeng Zhang³, Donghui Wu⁴, Deli Wang⁵

Affiliations

¹ Key Laboratory of Vegetation Ecology, Ministry of Education, Northeast Normal University, Changchun, 130024, China.
² USDA, Forest Service, Southern Research Station, Center for Forest Disturbance Science, Athens, GA 30602, USA.
³ Key Laboratory of Vegetation Ecology, Ministry of Education, Northeast Normal University, Changchun, 130024, China; Hebei Key Laboratory of Animal Diversity, Langfang Normal University, Langfang, 065000, China.
⁴ Key Laboratory of Vegetation Ecology, Ministry of Education, Northeast Normal University, Changchun, 130024, China; Jilin Provincial Key Laboratory of Animal Resource Conservation and Utilization, Northeast Normal University, Changchun, 130117, China; Key Laboratory of Wetland Ecology and Environment, Northeast Institute of Geography and Agroecology, Chinese Academy of Sciences, Changchun, 130102, China; Jilin Songnen Grassland Ecosystem National Observation and Research Station, Changchun, 130024, China. Electronic address: wudonghui@iga.ac.cn.
⁵ Key Laboratory of Vegetation Ecology, Ministry of Education, Northeast Normal University, Changchun, 130024, China; Jilin Songnen Grassland Ecosystem National Observation and Research Station, Changchun, 130024, China.

PMID: 37657540
DOI: 10.1016/j.scitotenv.2023.166666

Abstract

Adaptations to temperature and food resources, which can be affected by gut microbiota, are two main adaptive strategies allowing soil fauna to survive in their habitats, especially for cold-blooded animals. Earthworms are often referred to as ecosystem engineers because they make up the biggest component of the animal biomass found in the soil. They are considered as an important indicator in the triangle of soil quality, health and functions. However, the roles of gut microbiota in the environmental adaptation of earthworms at a large scale remain obscure. We explored the gut bacterial communities and their functions in the environmental adaptation of two widespread earthworm species (Eisenia nordenskioldi Eisen and Drawida ghilarovi Gates) in Northeast China (1661 km). Based on our findings, the alpha diversity of gut bacterial communities decreased with the increase of latitude, and the gut bacterial community composition was shaped by both mean annual temperature (MAT) and cellulose. Actinobacteria, Proteobacteria, Firmicutes, and Planctomycetes, recognized as the predominant cellulose degraders, were keystone taxa driving gut bacterial interactions. Actinobacteria, Firmicutes, and Planctomycetes were influenced by MAT and cellulose, and had higher contributions to gut total cellulase activity. The optimal temperature for total cellulase in the gut of E. nordenskioldi (25-30 °C) was lower than that of D ghilarovi (40 °C). The gut microbiota-deleted earthworms had the lowest cellulose degradation rate (1.07 %). The cellulose was degraded faster by gut bacteria from the host they were derived, indicating the presence of home field advantage of cellulose decomposition. This study provides a foundation for understanding the biotic strategies adopted by earthworms when they enter a new habitat, with gut microbiota being central to food digestion and environmental adaptability.

Keywords: Cellulose degradation; Ecosystem engineers; Symbiotic microorganism; Thermal adaptability.