Understanding the transmission of bacterial agents of sapronotic diseases using an ecosystem-based approach: A first spatially realistic metacommunity model
Pathogens such as bacteria, fungi and viruses are important components of soil and aquatic communities, where they can benefit from decaying and living organic matter, and may opportunistically infect human and animal hosts. One-third of human infectious diseases is constituted by sapronotic disease agents that are natural inhabitants of soil or aquatic ecosystems. They are capable of existing and reproducing in the environment outside of the host for extended periods of time. However, as ecological research on sapronosis is infrequent and epidemiological models are even rarer, very little information is currently available. Their importance is overlooked in medical and veterinary research, as well as the relationships between free environmental forms and those that are pathogenic. Here, using dynamical models in realistic aquatic metacommunity systems, we analyze sapronosis transmission, using the human pathogen Mycobacterium ulcerans that is responsible for Buruli ulcer. We show that the persistence of bacilli in aquatic ecosystems is driven by a seasonal upstream supply, and that the attachment and development of cells to aquatic living forms is essential for such pathogen persistence and population dynamics. Our work constitutes the first set of metacommunity models of sapronotic disease transmission, and is highly flexible for adaptation to other types of sapronosis. The importance of sapronotic agents on animal and human disease burden needs better understanding and new models of sapronosis disease ecology to guide the management and prevention of this important group of pathogens.
Authors
- Christine Chevillon (ORCID: https://orcid.org/0000-0002-1262-5839)
- Kayla M. Fast (ORCID: https://orcid.org/0000-0001-5476-5330)
- Michael J. Sandel (ORCID: https://orcid.org/0000-0001-9083-9202)
- Jennifer L. Pechal (ORCID: https://orcid.org/0000-0002-2588-2519)
- Matthew E. Scott (ORCID: https://orcid.org/0009-0009-9894-8599)
- M. Eric Benbow (ORCID: https://orcid.org/0000-0003-2630-0282)
- Magdalene Dogbe (ORCID: https://orcid.org/0000-0003-1533-6095)
- Ousmane Seydi (ORCID: https://orcid.org/0000-0001-5702-2575)
- Jean‐François Guégan (ORCID: https://orcid.org/0000-0002-7218-107X)
- Ahmadou Sylla (ORCID: https://orcid.org/0009-0008-3111-0604)
- Alex Rakestraw (ORCID: https://orcid.org/0000-0002-8087-0780)
- Heather R. Jordan (ORCID: https://orcid.org/0000-0002-4197-2194)
- Carlos Campos (ORCID: https://orcid.org/0000-0002-9644-3652)
- Ramsès Djidjiou-Demasse
Institutions
- Université Claude Bernard Lyon 1 (FR)
- Centre National de la Recherche Scientifique (FR)
- Maladies Infectieuses et Vecteurs: Écologie, Génétique, Évolution et Contrôle (FR)
- Institut National de Recherche pour l'Agriculture, l'Alimentation et l'Environnement (FR)
- VetAgro Sup (FR)
- Michigan United (US)
- Mississippi Department of Wildlife Fisheries and Parks (US)
- École Polytechnique de Thiès (SN)
- Institut de Recherche pour le Développement (FR)
- Michigan State University (US)
- Mississippi State University (US)
Publication Details
- Journal
- PLoS Computational Biology
- Published
- 2024-09-10
- DOI
- https://doi.org/10.1371/journal.pcbi.1012435
- Citations
- 4
- Primary Topic
- Mycobacterium research and diagnosis
- Type
- article
- Field-Weighted Citation Impact
- 1.55
Funders
- National Science Foundation
- Mississippi State University
- Michigan State University
- Centre Méditerranéen de l’Environnement et de la Biodiversité
- Agence Nationale de la Recherche
- Centre National de la Recherche Scientifique
- Institut National de Recherche pour l'Agriculture, l'Alimentation et l'Environnement
- National Institutes of Health
- National Institute of Food and Agriculture
- College of Engineering, Michigan State University