Disruption of termite gut-microbiota and its prolonged fitness consequences

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

Immunity in Society: Diverse Solutions to Common Problems

How do social animals, from insects to humans, limit the spread of disease by deploying community-level responses to pathogens? Active immunization of healthy ants by infected ants is one intriguing example

When Subterranean Termites Challenge the Rules of Fungal Epizootics

Over the past 50 years, repeated attempts have been made to develop biological control technologies for use against economically important species of subterranean termites, focusing primarily on the use of the entomopathogenic fungus Metarhizium anisopliae. However, no successful field implementation of biological control has been reported. Most previous work has been conducted under the assumption that environmental conditions within termite nests would favor the growth and dispersion of entomopathogenic agents, resulting in an epizootic. Epizootics rely on the ability of the pathogenic microorganism to self-replicate and disperse among the host population. However, our study shows that due to multilevel disease resistance mechanisms, the incidence of an epizootic within a group of termites is unlikely. By exposing groups of 50 termites in planar arenas containing sand particles treated with a range of densities of an entomopathogenic fungus, we were able to quantify behavioral patterns as a function of the death ratios resulting from the fungal exposure. The inability of the fungal pathogen M. anisopliae to complete its life cycle within a Coptotermes formosanus (Isoptera: Rhinotermitidae) group was mainly the result of cannibalism and the burial behavior of the nest mates, even when termite mortality reached up to 75%. Because a subterranean termite colony, as a superorganism, can prevent epizootics of M. anisopliae, the traditional concepts of epizootiology may not apply to this social insect when exposed to fungal pathogens, or other pathogen for which termites have evolved behavioral and physiological means of disrupting their life cycle

Social Transfer of Pathogenic Fungus Promotes Active Immunisation in Ant Colonies

Social contact with fungus-exposed ants leads to pathogen transfer to healthy nest-mates, causing low-level infections. These micro-infections promote pathogen-specific immune gene expression and protective immunization of nest-mates

Co-founding ant queens prevent disease by performing prophylactic undertaking behaviour

Abstract Background Social insects form densely crowded societies in environments with high pathogen loads, but have evolved collective defences that mitigate the impact of disease. However, colony-founding queens lack this protection and suffer high rates of mortality. The impact of pathogens may be exacerbated in species where queens found colonies together, as healthy individuals may contract pathogens from infectious co-founders. Therefore, we tested whether ant queens avoid founding colonies with pathogen-exposed conspecifics and how they might limit disease transmission from infectious individuals. Results Using Lasius niger queens and a naturally infecting fungal pathogen Metarhizium brunneum, we observed that queens were equally likely to found colonies with another pathogen-exposed or sham-treated queen. However, when one queen died, the surviving individual performed biting, burial and removal of the corpse. These undertaking behaviours were performed prophylactically, i.e. targeted equally towards non-infected and infected corpses, as well as carried out before infected corpses became infectious. Biting and burial reduced the risk of the queens contracting and dying from disease from an infectious corpse of a dead co-foundress. Conclusions We show that co-founding ant queens express undertaking behaviours that, in mature colonies, are performed exclusively by workers. Such infection avoidance behaviours act before the queens can contract the disease and will therefore improve the overall chance of colony founding success in ant queens

Discovery of a novel Wolbachia supergroup in Isoptera

Author Posting. © The Authors, 2005. This is the author's version of the work. It is posted here by permission of Springer-Verlag New York for personal use, not for redistribution. The definitive version was published in Current Microbiology 51 (2005): 393-398, doi:10.1007/s00284-005-0084-0.Wolbachia are one of the most abundant groups of bacterial endosymbionts in the biosphere. Interest in these heritable microbes has expanded with the discovery of wider genetic diversity in undersampled host species. Here, we report on the putative discovery of a new genetic lineage, denoted supergroup H, which infects the Isopteran species Zootermopsis angusticollis and Z. nevadensis. Evidence for this novel supergroup is based on portions of new Wolbachia gene sequences from each species spanning 3.5 kilobases of DNA and the following genes: 16S rDNA, dnaA, gltA, groEL, and ftsZ. Single-gene and concatenated maximum likelihood phylogenies establish this new supergroup and validate the positioning of the other Wolbachia supergroups. This discovery is the first example of a termite Wolbachia that is highly divergent from the Isopteran Wolbachia previously described in supergroup F. This study highlights the importance of multilocus approaches to resolving Wolbachia supergroup relationships. It also suggests that surveys of Wolbachia in more earlier-originating (and undersampled) groups of arthropods are more apt to reveal novel genetic diversity.This work was supported by grants from the NASA Astrobiology Institute (NNA04CC04A) and the Neal W. Cornell Endowed Research Fund

The development of immunity in a social insect: Evidence for the group facilitation of disease resistance

The extraordinary diversity and ecological success of the social insects has been attributed to their ability to cope with the rich and often infectious microbial community inhabiting their nests and feeding sites. Mechanisms of disease control used by eusocial species include antibiotic glandular secretions, mutual grooming, removal of diseased individuals from the nest, and the innate and adaptive immune responses of colony members. Here we demonstrate that after a challenge exposure to the entomopathogenic fungus Metarhizium anisopliae, dampwood termites Zootermopsis angusticollis have higher survivorship when individuals develop immunity as group members. Furthermore, termites significantly improve their ability to resist infection when they are placed in contact with previously immunized nestmates. This “social transfer” of infection resistance, a previously unrecognized mechanism of disease control in the social insects, could explain how group living may improve the survivorship of colony members despite the increased risks of pathogen transmission that can accompany sociality