Leishmania genetic exchange is mediated by IgM natural antibodies

Tiago D. Serafim (), Eva Iniguez, Ana Beatriz F. Barletta, Pedro Cecilio, Johannes S. P. Doehl, Mara Short, Justin Lack, Vinod Nair, Maria Disotuar, Timothy Wilson, Iliano V. Coutinho-Abreu, Claudio Meneses, John Andersen, Thiago Luiz Alves E Silva, Fabiano Oliveira, Joel Vega-Rodriguez, Carolina Barillas-Mury, José M. C. Ribeiro, Stephen M. Beverley (), Shaden Kamhawi () and Jesus G. Valenzuela ()
Additional contact information
Tiago D. Serafim: National Institutes of Health
Eva Iniguez: National Institutes of Health
Ana Beatriz F. Barletta: National Institutes of Health
Pedro Cecilio: National Institutes of Health
Johannes S. P. Doehl: National Institutes of Health
Mara Short: National Institutes of Health
Justin Lack: National Institutes of Health
Vinod Nair: National Institutes of Health
Maria Disotuar: National Institutes of Health
Timothy Wilson: National Institutes of Health
Iliano V. Coutinho-Abreu: National Institutes of Health
Claudio Meneses: National Institutes of Health
John Andersen: National Institutes of Health
Thiago Luiz Alves E Silva: National Institutes of Health
Fabiano Oliveira: National Institutes of Health
Joel Vega-Rodriguez: National Institutes of Health
Carolina Barillas-Mury: National Institutes of Health
José M. C. Ribeiro: National Institutes of Health
Stephen M. Beverley: Washington University
Shaden Kamhawi: National Institutes of Health
Jesus G. Valenzuela: National Institutes of Health

Nature, 2023, vol. 623, issue 7985, 149-156

Abstract: Abstract Host factors that mediate Leishmania genetic exchange are not well defined. Here we demonstrate that natural IgM (IgMn)1–4 antibodies mediate parasite genetic exchange by inducing the transient formation of a spherical parasite clump that promotes parasite fusion and hybrid formation. We establish that IgMn from Leishmania-free animals binds to the surface of Leishmania parasites to induce significant changes in the expression of parasite transcripts and proteins. Leishmania binding to IgMn is partially lost after glycosidase treatment, although parasite surface phosphoglycans, including lipophosphoglycan, are not required for IgMn-induced parasite clumping. Notably, the transient formation of parasite clumps is essential for Leishmania hybridization in vitro. In vivo, we observed a 12-fold increase in hybrid formation in sand flies provided a second blood meal containing IgMn compared with controls. Furthermore, the generation of recombinant progeny from mating hybrids and parental lines were only observed in sand flies provided with IgMn. Both in vitro and in vivo IgM-induced Leishmania crosses resulted in full genome hybrids that show equal patterns of biparental contribution. Leishmania co-option of a host natural antibody to facilitate mating in the insect vector establishes a new paradigm of parasite–host–vector interdependence that contributes to parasite diversity and fitness by promoting genetic exchange.

Date: 2023
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DOI: 10.1038/s41586-023-06655-8

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