Gut microbiome as a key monitoring indicator for reintroductions of captive animals

• Published in: Conservation biology 2024-02, Vol.38 (1), p.e14173-n/a
• Main Authors: Huang, Guangping, Qi, Dunwu, Yang, Zhisong, Hou, Rong, Shi, Wenyu, Zhao, Fangqing, Li, Zitian, Yan, Li, Wei, Fuwen
• Format: Article
• Language: English
• Subjects: Animals; Bacteria; Biodiversity; Biodiversity loss; biología de la conservación; Clostridium; conservation biology; Conservation of Natural Resources; Diet; Digestive system; Ecological succession; Escherichia; Evolution; Evolution & development; fauna; Feces; Gastrointestinal Microbiome; Gastrointestinal tract; gut microbiome; Humans; indicador de monitoreo; Intestinal flora; Intestinal microflora; Intestine; Metagenomics; microbioma intestinal; Microbiomes; Microorganisms; Monitoring; monitoring indicator; Pandas; Pseudomonas; Pseudomonas protegens; reintroducción; Reintroduction; Symbionts; Ursidae; wildlife; 保护生物学; 放归; 监测指标; 肠道微生物; 野生动物
• ISSN: 0888-8892; 1523-1739
• DOI: 10.1111/cobi.14173

Reintroduction programs seek to restore degraded populations and reverse biodiversity loss. To examine the hypothesis that gut symbionts could be used as an indicator of reintroduction success, we performed intensive metagenomic monitoring over 10 years to characterize the ecological succession and adaptive evolution of the gut symbionts of captive giant pandas reintroduced to the wild. We collected 63 fecal samples from 3 reintroduced individuals and 22 from 9 wild individuals and used 96 publicly available samples from another 3 captive individuals. By microbial composition analysis, we identified 3 community clusters of the gut microbiome (here termed enterotypes) with interenterotype succession that was closely related to the reintroduction process. Each of the 3 enterotypes was identified based on significant variation in the levels of 1 of 3 genera: Clostridium, Pseudomonas, and Escherichia. The enterotype of captive pandas was Escherichia. This enterotype was gradually replaced by the Clostridium enterotype during the wild‐training process, which in turn was replaced by the Pseudomonas enterotype that resembled the enterotype of wild pandas, an indicator of conversion to wildness and a successful reintroduction. We also isolated 1 strain of Pseudomonas protegens from the wild enterotype, a previously reported free‐living microbe, and found that its within‐host evolution contributed to host dietary adaptation in the wild. Monitoring gut microbial structure provides a novel, noninvasive tool that can be used as an indicator of successful reintroduction of a captive individual to the wild. Microbiomas intestinales como indicadores clave de monitoreo para la reintroducción de animales cautivos Resumen Los programas de reintroducción buscan restaurar las poblaciones degradadas y revertir la pérdida de la biodiversidad. Realizamos un monitoreo metagenómico intensivo durante más de diez años para caracterizar la sucesión ecológica y la evolución adaptativa de los simbiontes intestinales de pandas reintroducidos en la naturaleza y así comprobar la hipótesis de que estos simbiontes pueden usarse como indicadores de una reintroducción exitosa. Recolectamos 63 muestras fecales de tres individuos reintroducidos y 22 de nueve individuos silvestres y usamos 96 muestras disponibles al público de otros tres individuos cautivos. Mediante el análisis de la composición microbiana identificamos tres grupos comunitarios del microbioma intestinal (denominados como entero