Amphibian mucus triggers a developmental transition in the frog-killing chytrid fungus

Abstract

The frog-killing chytrid fungus Batrachochytrium dendrobatidis (Bd) is decimating amphibian populations around the world.1Skerratt L.F. Berger L. Speare R. Cashins S. McDonald K.R. Phillott A.D. Hines H.B. Kenyon N. Spread of Chytridiomycosis has caused the rapid global decline and extinction of frogs.EcoHealth. 2007; 4: 125Crossref Scopus (941) Google Scholar, 2Fisher M.C. Garner T.W.J. Walker S.F. Global emergence of Batrachochytrium dendrobatidis and amphibian chytridiomycosis in space, time, and host.Annu. Rev. Microbiol. 2009; 63: 291-310Crossref PubMed Scopus (520) Google Scholar, 3Scheele B.C. Pasmans F. Skerratt L.F. Berger L. Martel A. Beukema W. Acevedo A.A. Burrowes P.A. Carvalho T. Catenazzi A. et al.Amphibian fungal panzootic causes catastrophic and ongoing loss of biodiversity.Science. 2019; 363: 1459-1463Crossref PubMed Scopus (491) Google Scholar, 4Lambert M.R. Womack M.C. Byrne A.Q. Hernández-Gómez O. Noss C.F. Rothstein A.P. Blackburn D.C. Collins J.P. Crump M.L. Koo M.S. et al.Comment on “Amphibian fungal panzootic causes catastrophic and ongoing loss of biodiversity”.Science. 2020; 367: eaay1838Crossref PubMed Scopus (24) Google Scholar Bd has a biphasic life cycle, alternating between motile zoospores that disperse within aquatic environments and sessile sporangia that grow within the mucus-coated skin of amphibians.5Berger L. Hyatt A.D. Speare R. Longcore J.E. Life cycle stages of the amphibian chytrid Batrachochytrium dendrobatidis.Dis. Aquat. Organ. 2005; 68: 51-63Crossref PubMed Scopus (221) Google Scholar,6Longcore J.E. Pessier A.P. Nichols D.K. Batrachochytrium dendrobatidis gen. et sp. nov., a chytrid pathogenic to amphibians.Mycologia. 1999; 91: 219-227Crossref Scopus (946) Google Scholar Zoospores lack cell walls and swim rapidly through aquatic environments using a posterior flagellum and crawl across solid surfaces using actin structures similar to those of human cells.7Prostak S.M. Robinson K.A. Titus M.A. Fritz-Laylin L.K. The actin networks of chytrid fungi reveal evolutionary loss of cytoskeletal complexity in the fungal kingdom.Curr. Biol. 2021; 31: 1192-1205.e6Abstract Full Text Full Text PDF PubMed Scopus (8) Google Scholar,8Fritz-Laylin L.K. Lord S.J. Mullins R.D. WASP and SCAR are evolutionarily conserved in actin-filled pseudopod-based motility.J. Cell Biol. 2017; 216: 1673-1688Crossref PubMed Scopus (59) Google Scholar Bd transitions from this motile dispersal form to its reproductive form by absorbing its flagellum, rearranging its actin cytoskeleton, and rapidly building a chitin-based cell wall—a process called “encystation.”5Berger L. Hyatt A.D. Speare R. Longcore J.E. Life cycle stages of the amphibian chytrid Batrachochytrium dendrobatidis.Dis. Aquat. Organ. 2005; 68: 51-63Crossref PubMed Scopus (221) Google Scholar, 6Longcore J.E. Pessier A.P. Nichols D.K. Batrachochytrium dendrobatidis gen. et sp. nov., a chytrid pathogenic to amphibians.Mycologia. 1999; 91: 219-227Crossref Scopus (946) Google Scholar, 7Prostak S.M. Robinson K.A. Titus M.A. Fritz-Laylin L.K. The actin networks of chytrid fungi reveal evolutionary loss of cytoskeletal complexity in the fungal kingdom.Curr. Biol. 2021; 31: 1192-1205.e6Abstract Full Text Full Text PDF PubMed Scopus (8) Google Scholar The resulting sporangium increases in volume by two or three orders of magnitude while undergoing rounds of mitosis without cytokinesis to form a large ceonocyte. The sporangium then cellurizes by dividing its cytoplasm into dozens of new zoospores. After exiting the sporangium through a discharge tube onto the amphibian skin, daughter zoospores can then reinfect the same individual or find a new host.5Berger L. Hyatt A.D. Speare R. Longcore J.E. Life cycle stages of the amphibian chytrid Batrachochytrium dendrobatidis.Dis. Aquat. Organ. 2005; 68: 51-63Crossref PubMed Scopus (221) Google Scholar Although encystation is critical to Bd growth, whether and how this developmental transition is triggered by external signals was previously unknown. We discovered that exposure to amphibian mucus triggers rapid and reproducible encystation within minutes. This response can be recapitulated with purified mucin, the bulk component of mucus, but not by similarly viscous methylcellulose or simple sugars. Mucin-induced encystation does not require gene expression but does require surface adhesion, calcium signaling, and modulation of the actin cytoskeleton. Mucus-induced encystation may represent a key mechanism for synchronizing Bd development with the arrival at the host.

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