Biotic interactions and environmental modifications determine symbiotic microbial diversity and stability

Abstract

Taking amphibians as island models, we examined the effects of interspecific interaction on the diversity and stability of microbial ecological. As skin area increased, the diversity and stability of skin microbes decreased, but the strength of negative interactions increased significantly. In contrast, as gut area increased, the diversity and stability of gut microbes increased, but the strength of interactions remained constant. These results indicate that microbial interactions are affected by habitat properties. When living in fluctuating environments without strong filtering, microorganisms can enhance their negative interactions with other taxa by changing the pH of their surroundings. In contrast, the pH of the gut is relatively stable, and colonized microorganisms cannot alter the gut pH and inhibit other colonizers. This study demonstrates that in the field of microbiology, diversity and stability are predominantly influenced by the intensity of interspecies interactions. The findings in this study deepen our understanding of microbial diversity and stability and provide a mechanistic link between species interactions, biodiversity, and stability in microbial ecosystems.

Keywords: Empirical networks; Environmental modification; Microbial diversity-area relationship (MDAR); Microbial stability-area relationship (MSAR).

Graphical abstract

Fig. 1

Geometric transformation and calculation of the microhabitat area size of amphibian hosts. (A) A geometric model for skin microhabitat area surface size calculation; (B) a geometric model for gut habitat area surface size calculation.

Fig. 2

Dynamics of the relative abundance of the bacteriome with habitat area. Only the taxa that were detected in at least 10 % of all samples per group are shown at the phylum level. (A) The shifts in taxonomic composition of the skin microbial community with habitat area. (B) The shifts in taxonomic composition of the gut microbial community with habitat area. (Small skin colonizers: significantly decreased with increasing skin area; Big gut colonizers: significantly increased with increasing gut area; complex: not changed with habitat area).

Fig. 3

Overall relationship between symbiotic microbial diversity (measured using the order of Hill number [q = 0, 1, 2, 3]) and habitat area sizes (mm²). (A) Amphibian skin microbial diversity-area relationship. (B) Amphibian gut microbial diversity-area relationship.

Fig. 4

Correlations between habitat area and network topological properties. (A) Network topological properties of amphibian skin microbes in relation to skin area. (B) Network topological properties of amphibian gut microbes in relation to skin area.

Fig. 5

Trends in network stability along with habitat area. Robustness-random was measured as the proportion of taxa that remained with 50 % of the taxa randomly removed from each network. Robustness-target was measured as the proportion of taxa that remained with certain numbers of key nodes removed from each of the networks. Network resistance was measured as the ability of the network to maintain connectivity after the removal of nodes. Network vulnerability was measured by the maximum node vulnerability in each network.

Fig. 6

Cohesion of microbial communities and their relationships with habitat area. (A) Changes in the positive cohesion of the skin microbial community along the skin area gradient. (B) Changes in the negative cohesion of the skin microbial community along the skin area gradient. (C) Changes in the ratio of negative:positive cohesion of gut microbes along the skin area gradient. (D) Changes in the positive cohesion of the gut microbial community along the gut area gradient. (E) Changes in the negative cohesion of the gut microbial community along the gut area gradient. (F) Changes in the ratio of negative:positive cohesion of gut microbes along the gut area gradient.