Microbial Grazers May Aid in Controlling Infections Caused by the Aquatic Zoosporic Fungus Batrachochytrium dendrobatidis.

Matthew C. Fisher,Trent W. J. Garner,Hazel N. Farthing,Jiamei Jiang,David J. S. Montagnes,David R. Daversa,Andy Fenton,Alexandra J. Henwood

doi:10.3389/fmicb.2020.592286

Abstract

Free-living eukaryotic microbes may reduce animal diseases. We evaluated the dynamics by which micrograzers (primarily protozoa) apply top-down control on the chytrid Batrachochytrium dendrobatidis (Bd) a devastating, panzootic pathogen of amphibians. Although micrograzers consumed zoospores (∼3 μm), the dispersal stage of chytrids, not all species grew monoxenically on zoospores. However, the ubiquitous ciliate Tetrahymena pyriformis, which likely co-occurs with Bd, grew at near its maximum rate (r = 1.7 d–1). A functional response (ingestion vs. prey abundance) for T. pyriformis, measured using spore-surrogates (microspheres) revealed maximum ingestion (Imax) of 1.63 × 103 zoospores d–1, with a half saturation constant (k) of 5.75 × 103 zoospores ml–1. Using these growth and grazing data we developed and assessed a population model that incorporated chytrid-host and micrograzer dynamics. Simulations using our data and realistic parameters obtained from the literature suggested that micrograzers could control Bd and potentially prevent chytridiomycosis (defined as 104 sporangia host–1). However, simulated inferior micrograzers (0.7 × Imax and 1.5 × k) did not prevent chytridiomycosis, although they ultimately reduced pathogen abundance to below levels resulting in disease. These findings indicate how micrograzer responses can be applied when modeling disease dynamics for Bd and other zoosporic fungi.

Highlights

The traditional microbial food web (i.e., prokaryotes and protists, sensu Azam et al (1983) is well-established as a driver of aquatic productivity (Fenchel, 1987), fungi are only being appreciated as integral aquatic microbes
We indicate the dynamics by which micrograzers may reduce Batrachochytrium dendrobatidis (Bd) populations – potentially preventing disease – and provide a mechanism by which chytrid-diseases can be incorporated into microbial food web models
As T. pyriformis grew on zoospores alone it was clear that this ciliate ingested, digested, and assimilated Bd zoospores

Summary

Introduction

The traditional microbial food web (i.e., prokaryotes and protists, sensu Azam et al (1983) is well-established as a driver of aquatic productivity (Fenchel, 1987), fungi are only being appreciated as integral aquatic microbes. Through top-down control micrograzers within the Disease Control by Micrograzers microbial food web have the potential to reduce the likelihood or severity of, or even prevent, disease outbreaks caused by these pathogens (Kagami et al, 2014; Grossart and RojasJimenez, 2016; Frenken et al, 2019). By developing and parameterizing a population model we explore the dynamics by which microbial grazers may control the chytrid Batrachochytrium dendrobatidis, a panzootic pathogen of amphibians that is argued to have caused the greatest loss of biodiversity attributed to any disease (Scheele et al, 2019). Experiments show that some micrograzers may reduce the likelihood of Bd infections, and field data indicate a negative relationship between potential-grazer abundance and both the prevalence of infection and host mortality from disease (Woodhams et al, 2008; Buck et al, 2011; Gleason et al, 2014; Schmeller et al, 2014).

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Conclusion