Disruption of termite gut-microbiota and its prolonged fitness consequences

Abstract

Author Posting. © The Author(s), 2011. This is the author's version of the work. It is posted here by permission of American Society for Microbiology for personal use, not for redistribution. The definitive version was published in Applied and Environmental Microbiology 77 (2011): 4303-4312, doi:10.1128/AEM.01886-10.The disruption of host-symbiont interactions through the use of antibiotics can help elucidate microbial functions that go beyond short-term nutritional value. Termite gut symbionts have been studied extensively, but little is known about their impact on the termite’s reproductive output. Here we describe the effect that the antibiotic rifampin has not only on the gut microbial diversity, but also on the longevity, fecundity, and weight of two termite species - Zootermopsis angusticollis and Reticulitermes flavipes. We report three key findings: (i) the antibiotic rifampin, when fed to primary reproductives during the incipient stages of colony foundation, causes a permanent reduction in the diversity of gut bacteria, and a transitory effect on the density of the protozoan community, (ii) rifampin treatment reduces oviposition rates of queens, translating into delayed colony growth and ultimately reduced colony fitness and (iii) the initial dosages of rifampin on reproduction and colony fitness had severe longterm fitness effects on Z. angusticollis survivorship and colony size. Taken together, our findings demonstrate that the antibiotic-induced perturbation of the microbial community associates with prolonged reductions in longevity and fecundity. A causal relationship between these changes in the gut microbial population structures and fitness is suggested by the acquisition of opportunistic pathogens and incompetence of the termites to restore a pre-treatment, native microbiota. Our results indicate that antibiotic treatment significantly alters the termite’s microbiota, reproduction, colony establishment and ultimately, colony growth and development. We discuss the implications for antimicrobials as a new application to the control of termite pest species.This research was funded by the Louis Stokes Minority Program which supported Jessica Dumas, NSF CAREER award DEB 0447316 to Rosengaus RB, and NSF IOS-0852344 and NAI NNA04CC04A to Bordenstein SR