Spores and soil from six sides: interdisciplinarity and the environmental biology of anthrax (Bacillus anthracis)

Abstract

Environmentally transmitted diseases are comparatively poorly understood and managed, and their ecology is particularly understudied. Here we identify challenges of studying environmental transmission and persistence with a six-sided interdisciplinary review of the biology of anthrax (Bacillus anthracis). Anthrax is a zoonotic disease capable of maintaining infectious spore banks in soil for decades (or even potentially centuries), and the mechanisms of its environmental persistence have been the topic of significant research and controversy. Where anthrax is endemic, it plays an important ecological role, shaping the dynamics of entire herbivore communities. The complex eco-epidemiology of anthrax, and the mysterious biology of Bacillus anthracis during its environmental stage, have necessitated an interdisciplinary approach to pathogen research. Here, we illustrate different disciplinary perspectives through key advances made by researchers working in Etosha National Park, a long-term ecological research site in Namibia that has exemplified the complexities of the enzootic process of anthrax over decades of surveillance. In Etosha, the role of scavengers and alternative routes (waterborne transmission and flies) has proved unimportant relative to the long-term * Authors for correspondence: (Colin J. Carlson-Tel.: +1 (510) 990 2258; E-mail: ccarlson@sesync.org; Wayne M. Getz-Tel.: +1 510 642 8745; E-mail: wgetz@berkeley.edu; Nils C. Stenseth-Tel.: +47-22854584/+47-22854400; E-mail: n.c.stenseth@ibv.uio.no).Biological Reviews (2018) 000-000 © 2018 Cambridge Philosophical Society 2 Colin J. Carlson and others persistence of anthrax spores in soil and their infection of herbivore hosts. Carcass deposition facilitates green-ups of vegetation to attract herbivores, potentially facilitated by the role of anthrax spores in the rhizosphere. The underlying seasonal pattern of vegetation, and herbivores' immune and behavioural responses to anthrax risk, interact to produce regular 'anthrax seasons' that appear to be a stable feature of the Etosha ecosystem. Through the lens of microbiologists, geneticists, immunologists, ecologists, epidemiologists, and clinicians, we discuss how anthrax dynamics are shaped at the smallest scale by population genetics and interactions within the bacterial communities up to the broadest scales of ecosystem structure. We illustrate the benefits and challenges of this interdisciplinary approach to disease ecology, and suggest ways anthrax might offer insights into the biology of other important pathogens. Bacillus anthracis, and the more recently emerged Bacillus cereus biovar anthracis, share key features with other environmentally transmitted pathogens, including several zoonoses and panzootics of special interest for global health and conservation efforts. Understanding the dynamics of anthrax, and developing interdisciplinary research programs that explore environmental persistence, is a critical step forward for understanding these emerging threats.

Synergistic China–US Ecological Research is Essential for Global Emerging Infectious Disease Preparedness

“…This region experienced no outbreaks of dengue-like illness from the period of 1950-1977, followed by a relatively low level of incidence until a large-scale outbreak occurred in 2014, infecting over 45,000 people . Similarly, climate change is projected to impact the distribution of vector-borne disease in the USA, with the environment being more suitable for the introduction of Zika virus in certain regions of the southeastern USA (Carlson et al 2018). The combined US-China resource capacity is critical to better understand and mitigate anthropogenic EID drivers, such as urbanization, biodiversity loss, landscape conversion, intensive farming and climate change that are contributing to the spread of disease across the wildlife-livestock-human health continuum.…”

“…Collaborative research between China and the USA could greatly advance spatiotemporal disease prediction schemes because both countries encompass large climatic gradients, have high capacity for ecological and climatic data collection, and share some overlapping vectors, and zoonotic pathogens ; Estrada-Pena A complete understanding of host-pathogen interactions and how and where to intervene requires an ecosystem or ''One Health'' viewpoint that accounts for processes occurring at both macro-and micro-scales, including at the pathogen, host and environmental levels, as well as an integration of the effects of processes across these scales (Alexander et al 2018;Forst 2010;Blackburn et al 2019). Such multiscale ''One Health'' research requires the incorporation of many disciplines including, but not limited to, human medicine, veterinary medicine, public health, environmental science, ecology, conservation biology, nursing, social sciences, the humanities, engineering, economics, education and public policy Carlson et al 2018). China and the USA have led response activities for several epidemic and pandemic outbreaks impacting humans and animals which have required a One Health perspective.…”

“…While we currently do not have the ability to accurately forecast the time and location of the next EID outbreak, existing predictive models have been instrumental in prioritizing efforts. These include focusing on: sub-national regions (Allen et al 2017;Jones et al 2008); underlying environmental drivers (Allen et al 2017;Johnson et al 2015); specific reservoir host species (Olival et al 2017); and pathogen traits (Olival et al 2017;Fearnley et al 2019) that facilitate spillover (Carlson et al 2018). With a larger investment in disease ecology training in countries likely to be hot spots for EIDs, we can create the next generation of modeling and analytical techniques that incorporate more robust input from EID source nations.…”

A classification framework forBacillus anthracisdefined by global genomic structure

“…anthracis are primarily relegated to wild and domestic herbivores, with occasional spillover to humans (Carlson et al, 2018;de Vos et al, 2018). B. anthracis has also garnered global attention as a bioterrorism weapon due to the highly resilient qualities of its endospores, and their ability to be aerosolized for malicious purposes (Mugavero et al, 2015;Koehler & Popella, 2018).…”

Using movement data to estimate contact rates in a simulated environmentally-transmitted disease system

“…Here we develop an ABM for herbivore movement on an anthrax-endemic landscape, parameterized with empirical movement data. As anthrax is transmitted primarily through environmental reservoirs [33,34,35], we use the output of the model to estimate the probability of contact between agents and fixed environmental reservoirs (anthrax spores deposited at carcass sites), an important epidemiological rate that is highly dependent on the heterogeneity in individual movement. Rather than explicitly simulating the disease transmission process, we only aim to estimate contact rates between a host and an infectious agent.…”