Antibiotics and fecal transfaunation differentially affect microbiota recovery, associations, and antibiotic resistance in lemur guts

Abstract

Abstract Background Antibiotics alter the diversity, structure, and dynamics of host-associated microbial consortia, including via development of antibiotic resistance; however, patterns of recovery from microbial imbalances and methods to mitigate associated negative effects remain poorly understood, particularly outside of human-clinical and model-rodent studies that focus on outcome over process. To improve conceptual understanding of host-microbe symbiosis in more naturalistic contexts, we applied an ecological framework to a non-traditional, strepsirrhine primate model via long-term, multi-faceted study of microbial community structure before, during, and following two experimental manipulations. Specifically, we administered a broad-spectrum antibiotic, either alone or with subsequent fecal transfaunation, to healthy, male ring-tailed lemurs (Lemur catta), then used 16S rRNA and shotgun metagenomic sequencing to longitudinally track the diversity, composition, associations, and resistomes of their gut microbiota both within and across baseline, treatment, and recovery phases. Results Antibiotic treatment resulted in a drastic decline in microbial diversity and a dramatic alteration in community composition. Whereas microbial diversity recovered rapidly regardless of experimental group, patterns of microbial community composition reflected long-term instability following treatment with antibiotics alone, a pattern that was attenuated by fecal transfaunation. Covariation analysis revealed that certain taxa dominated bacterial associations, representing potential keystone species in lemur gut microbiota. Antibiotic resistance genes, which were universally present, including in lemurs that had never been administered antibiotics, varied across individuals and treatment groups. Conclusions Long-term, integrated study post antibiotic-induced microbial imbalance revealed differential, metric-dependent evidence of recovery, with beneficial effects of fecal transfaunation on recovering community composition, and potentially negative consequences to lemur resistomes. Beyond providing new perspectives on the dynamics that govern host-associated communities, particularly in the Anthropocene era, our holistic study in an endangered species is a first step in addressing the recent, interdisciplinary calls for greater integration of microbiome science into animal care and conservation.