Flexible host–microbe interaction aid adaptation of black-necked crane to seasonal shifts

Abstract

To elucidate how hosts adapt to changing environments with the assistance of symbiotic microorganisms, we must first understand host–microbe interactions. However, the covariation patterns of gut microbiota and hosts under complex natural conditions are poorly understood. To address this gap in our knowledge, we used metabarcoding of plant RbcL and animal COI regions, along with bacterial 16S rRNA gene and metagenomic analyses. This enabled the analysis of the interactions between the gut microbiota of the black-necked crane (Grus nigricollis), a large migratory bird, and its plant and animal diets to be analyzed. The impact of these interactions on the adaptive strategies of the black-necked crane during different periods in the Zoige wetland, China, was also assessed. We found that the black-necked crane harbored more gut bacterial communities and more diverse plant-derived foods during the post-breeding period than during the pre-breeding period. The gut microbiota and diet covaried throughout the breeding season and exhibited seasonal patterns. Araneae and Cyperaceae were correlated with pre-breeding bacterial profile, whereas Acrididae and Elaeagnaceae were associated with post-breeding bacterial abundance. Sample microbiota distance (between-sample diversity) increased with increasing animal and plant diet distance, and this relationship was enhanced between the plant diet and gut microbiome, with a greater value observed during the pre-breeding period than during the post-breeding period. According to Simpson's indexes, the gut microbiota was also positively associated with the plant-based diet across the seasons. The plant diet–microbe co-occurrence network was more complex than the animal diet–microbe network. The gut microbiota functional profile revealed that several amino acids, folate, lipids, and metabolic pathways were more abundant during the pre-breeding period, which enriched the nutrient resources of the black-necked crane prior to breeding. In contrast, carbohydrate metabolism was more abundant during the post-breeding period, which helped the black-necked crane to accumulate energy for its upcoming migration. These results suggest flexible host-microbiome-host relationships in two seasons and that host physiological needs interact with foraging strategies to shape the microbiome, ultimately resulting in host adaptations to seasonal shifts. These results provide insights into the role of the gut microbiota in host adaptations to seasonal changes under natural conditions.