Microsporidia with Vertical Transmission Were Likely Shaped by Nonadaptive Processes

Author:

Haag Karen L1,Pombert Jean-François2,Sun Yukun2,de Albuquerque Nathalia Rammé M1,Batliner Brendan2,Fields Peter3,Lopes Tiago Falcon1,Ebert Dieter3

Affiliation:

1. Department of Genetics and Post-Graduation Program of Genetics and Molecular Biology, Federal University of Rio Grande do Sul, Porto Alegre, Brazil

2. Department of Biology, Illinois Institute of Technology

3. Department of Environmental Sciences, Zoology, Basel University, Switzerland

Abstract

Abstract Microsporidia have the leanest genomes among eukaryotes, and their physiological and genomic simplicity has been attributed to their intracellular, obligate parasitic life-style. However, not all microsporidia genomes are small or lean, with the largest dwarfing the smallest ones by at least an order of magnitude. To better understand the evolutionary mechanisms behind this genomic diversification, we explore here two clades of microsporidia with distinct life histories, Ordospora and Hamiltosporidium, parasitizing the same host species, Daphnia magna. Based on seven newly assembled genomes, we show that mixed-mode transmission (the combination of horizontal and vertical transmission), which occurs in Hamiltosporidium, is found to be associated with larger and AT-biased genomes, more genes, and longer intergenic regions, as compared with the exclusively horizontally transmitted Ordospora. Furthermore, the Hamiltosporidium genome assemblies contain a variety of repetitive elements and long segmental duplications. We show that there is an excess of nonsynonymous substitutions in the microsporidia with mixed-mode transmission, which cannot be solely attributed to the lack of recombination, suggesting that bursts of genome size in these microsporidia result primarily from genetic drift. Overall, these findings suggest that the switch from a horizontal-only to a mixed mode of transmission likely produces population bottlenecks in Hamiltosporidium species, therefore reducing the effectiveness of natural selection, and allowing their genomic features to be largely shaped by nonadaptive processes.

Funder

Swiss National Science Foundation

Conselho Nacional de Desenvolvimento Científico e Tecnológico

National Institute of Allergy and Infectious Diseases of the National Institutes of Health

Publisher

Oxford University Press (OUP)

Subject

Genetics,Ecology, Evolution, Behavior and Systematics

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