Spatiotemporal plasticity of the gut microbiome facilitates redbelly tilapia (Coptodon zillii) invasion in China.

Abstract

Background: The redbelly tilapia (Coptodon zillii) is a highly invasive fish species posing serious ecological risks to freshwater systems in China. To uncover mechanisms behind its invasion success, this study investigated spatiotemporal plasticity of its gut microbiome and explored the drivers of such plasticity. Using high-throughput 16 S rRNA sequencing, gut microbiota of C. zillii from five water bodies (two rivers, three reservoirs) and from Shuikou Reservoir across four seasons were compared.

Results: Among populations from different habitats, 6 of the top 10 abundant phyla and 17 of the top 30 genera varied significantly (P < 0.05). Gut microbiota differed significantly (P < 0.05) in all pairwise population comparisons. Alpha diversity indices also showed significant differences among some populations (P < 0.05). Of 24 digestion-related KEGG pathways identified, 23 exhibited significant abundance variations across populations. Relative gene abundances of beta-glucosidase (P = 0.0025) and chitinase (P = 0.022) also differed significantly. Water temperature, dissolved oxygen, and conductivity were key environmental drivers of gut microbiota variation. Notably, microbial community assembly was predominantly governed by deterministic processes (> 60%), with heterogeneous selection contributing 42%-63%. In seasonal samples from Shuikou Reservoir, 6 of the top 10 phyla and 15 of the top 30 genera showed significant seasonal variation (P < 0.05). PERMANOVA indicated significant differences (P < 0.05) in all pairwise seasonal comparisons. Of 19 digestion-related KEGG pathways, 13 exhibited significant abundance variations across seasons. Chitinase-coding gene abundance varied significantly among populations (P < 0.0001). Key factors driving seasonal differentiation were pH, conductivity, turbidity degree, and total nitrogen.

Conclusions: The gut microbiome of invasive C. zillii displays significant spatiotemporal variation in structure, diversity, and functional gene composition. This pronounced plasticity-rather than a stable, specialized microbiota-likely serves as a key adaptive strategy, enabling the species to thrive in heterogeneous environments.