Understanding the transmission of bacterial agents of sapronotic diseases using an ecosystem-based approach: A first spatially realistic metacommunity model

PLoS Comput Biol. 2024 Sep 10;20(9):e1012435. doi: 10.1371/journal.pcbi.1012435. eCollection 2024 Sep.

Abstract

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.

MeSH terms

  • Animals
  • Buruli Ulcer / microbiology
  • Buruli Ulcer / transmission
  • Computational Biology
  • Ecosystem*
  • Humans
  • Models, Biological
  • Mycobacterium ulcerans / pathogenicity

Grants and funding

The authors are supported by two “Investissement d'Avenir” grants from the Agence Nationale de la Recherche (CEBA ANR-10-LABX-2501 and CEMEB ANR-10-LABX-0401). All authors are supported by the joint NSF-NIH-NIFA Ecology and Evolution of Infectious Disease program [DEB 1911457]. AS received a postdoctoral fellowship from DEB 1911457 and MEB received a visiting professor fellowship from LabEx CEMEB. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.