Mycobacterium ulcerans dynamics in aquatic ecosystems are driven by a complex interplay of abiotic and biotic factors

Abstract

Host–parasite interactions are often embedded within complex host communities and can be influenced by a variety of environmental factors, such as seasonal variations in climate or abiotic conditions in water and soil, which confounds our understanding of the main drivers of many multi-host pathogens. Here, we take advantage of a combination of large environmental data sets on Mycobacterium ulcerans (MU), an environmentally persistent microorganism associated to freshwater ecosystems and present in a large variety of aquatic hosts, to characterize abiotic and biotic factors driving the dynamics of this pathogen in two regions of Cameroon. We find that MU dynamics are largely driven by seasonal climatic factors and certain physico-chemical conditions in stagnant and slow-flowing ecosystems, with an important role of pH as limiting factor. Furthermore, water conditions can modify the effect of abundance and diversity of aquatic organisms on MU dynamics, which suggests a different contribution of two MU transmission routes for aquatic hosts (trophic vs environmental transmission) depending on local abiotic factors.Mycobacterium ulcerans is a slow-growing bacterium that causes a rare tropical disease in humans called Buruli ulcer. The infection affects the skin and underlying tissues, initially causing small painless lesions that can develop into large open sores or ulcers that are responsible for significant handicap in rural areas of sub-Saharan Africa.Disease outbreaks generally occur in close association with stagnant and slow-flowing aquatic ecosystems, mostly after floods or other large environmental disturbances. It is believed that contact with water sources that contain the bacteria causes infection in humans, but the specific mode of transmission remains a mystery. By defining the factors that influence the bacteria's presence in the environment, public health officials could develop initiatives that would reduce an individual's risk of infection when conditions support a M. ulcerans outbreak.To identify the environmental conditions that affect the prevalence of M. ulcerans in two regions of Cameroon where Buruli ulcer is present, Garchitorena et al. have now analyzed a large amount of ecological data about the bacteria using cutting-edge statistical techniques. This revealed that the amount of M. ulcerans varies following seasonal changes in climate, at least in the region dominated by tropical rainforest. In this region, the bacteria are also generally present in waters that are more alkaline and contain fewer animals, especially from certain species that could prevent the infection spreading to other aquatic hosts. In the other region, dominated by a savannah landscape, the bacteria are most abundant in stagnant or slowly moving waters that have optimal physical and chemical conditions and contain many diverse species of potential animal hosts. The discovery of contrasting results for the two regions suggests that there are at least two ways that M. ulcerans can persist in the environment and infect the aquatic animals. The prevailing method—through environmental transmission or through interactions between hosts—depends on the properties of the water.Many other infectious diseases are caused by pathogens that, like M. ulcerans, infect many different hosts and persist in the environment for long periods. Future research following methods like those used by Garchitorena et al. would help to reveal whether these pathogens are affected by environmental factors in similar ways to M. ulcerans.