Clonality despite sex: the evolution of host-associated sexual neighborhoods in the pathogenic fungus penicillium marneffei

Daniel A Henk, R. Shahar-Golan, K.R. Devi, K.J. Boyce, N. Zhan, N.D. Fedorova, W.C. Nierman, P.R. Hsueh, K.Y. Yuen, T.P.M. Sieu, Nguyen Van Kinh, Heiman Wertheim, Stephen G. Baker, Jeremy N. Day, Nongnuch Vanittanakom, Elaine M. Bignell, Alex Andrianopoulos, Matthew C. Fisher

Research output: Contribution to journalArticle

29 Citations (Scopus)

Abstract

Molecular genetic approaches typically detect recombination in microbes regardless of assumed asexuality. However, genetic data have shown the AIDS-associated pathogen Penicillium marneffei to have extensive spatial genetic structure at local and regional scales, and although there has been some genetic evidence that a sexual cycle is possible, this haploid fungus is thought to be genetically, as well as morphologically, asexual in nature because of its highly clonal population structure. Here we use comparative genomics, experimental mixed-genotype infections, and population genetic data to elucidate the role of recombination in natural populations of P. marneffei. Genome wide comparisons reveal that all the genes required for meiosis are present in P. marneffei, mating type genes are arranged in a similar manner to that found in other heterothallic fungi, and there is evidence of a putatively meiosis-specific mutational process. Experiments suggest that recombination between isolates of compatible mating types may occur during mammal infection. Population genetic data from 34 isolates from bamboo rats in India, Thailand and Vietnam, and 273 isolates from humans in China, India, Thailand, and Vietnam show that recombination is most likely to occur across spatially and genetically limited distances in natural populations resulting in highly clonal population structure yet sexually reproducing populations. Predicted distributions of three different spatial genetic clusters within P. marneffei overlap with three different bamboo rat host distributions suggesting that recombination within hosts may act to maintain population barriers within P. marneffei.
Original languageEnglish
Article numbere1002851
JournalPLoS Pathogens
Volume8
Issue number10
DOIs
Publication statusPublished - 4 Oct 2012

Fingerprint

Penicillium
Fungi
Genetic Recombination
Population
Vietnam
Meiosis
Population Genetics
Thailand
India
Genetic Structures
Haploidy
Genomics
Coinfection
Genes
Molecular Biology
Mammals
China
Acquired Immunodeficiency Syndrome
Genotype
Genome

Cite this

Clonality despite sex: the evolution of host-associated sexual neighborhoods in the pathogenic fungus penicillium marneffei. / Henk, Daniel A; Shahar-Golan, R.; Devi, K.R.; Boyce, K.J.; Zhan, N.; Fedorova, N.D.; Nierman, W.C.; Hsueh, P.R.; Yuen, K.Y.; Sieu, T.P.M.; Van Kinh, Nguyen; Wertheim, Heiman; Baker, Stephen G.; Day, Jeremy N.; Vanittanakom, Nongnuch; Bignell, Elaine M.; Andrianopoulos, Alex; Fisher, Matthew C.

In: PLoS Pathogens, Vol. 8, No. 10, e1002851, 04.10.2012.

Research output: Contribution to journalArticle

Henk, DA, Shahar-Golan, R, Devi, KR, Boyce, KJ, Zhan, N, Fedorova, ND, Nierman, WC, Hsueh, PR, Yuen, KY, Sieu, TPM, Van Kinh, N, Wertheim, H, Baker, SG, Day, JN, Vanittanakom, N, Bignell, EM, Andrianopoulos, A & Fisher, MC 2012, 'Clonality despite sex: the evolution of host-associated sexual neighborhoods in the pathogenic fungus penicillium marneffei', PLoS Pathogens, vol. 8, no. 10, e1002851. https://doi.org/10.1371/journal.ppat.1002851
Henk, Daniel A ; Shahar-Golan, R. ; Devi, K.R. ; Boyce, K.J. ; Zhan, N. ; Fedorova, N.D. ; Nierman, W.C. ; Hsueh, P.R. ; Yuen, K.Y. ; Sieu, T.P.M. ; Van Kinh, Nguyen ; Wertheim, Heiman ; Baker, Stephen G. ; Day, Jeremy N. ; Vanittanakom, Nongnuch ; Bignell, Elaine M. ; Andrianopoulos, Alex ; Fisher, Matthew C. / Clonality despite sex: the evolution of host-associated sexual neighborhoods in the pathogenic fungus penicillium marneffei. In: PLoS Pathogens. 2012 ; Vol. 8, No. 10.
@article{b74a415c8b344f4aae58960a97d23508,
title = "Clonality despite sex: the evolution of host-associated sexual neighborhoods in the pathogenic fungus penicillium marneffei",
abstract = "Molecular genetic approaches typically detect recombination in microbes regardless of assumed asexuality. However, genetic data have shown the AIDS-associated pathogen Penicillium marneffei to have extensive spatial genetic structure at local and regional scales, and although there has been some genetic evidence that a sexual cycle is possible, this haploid fungus is thought to be genetically, as well as morphologically, asexual in nature because of its highly clonal population structure. Here we use comparative genomics, experimental mixed-genotype infections, and population genetic data to elucidate the role of recombination in natural populations of P. marneffei. Genome wide comparisons reveal that all the genes required for meiosis are present in P. marneffei, mating type genes are arranged in a similar manner to that found in other heterothallic fungi, and there is evidence of a putatively meiosis-specific mutational process. Experiments suggest that recombination between isolates of compatible mating types may occur during mammal infection. Population genetic data from 34 isolates from bamboo rats in India, Thailand and Vietnam, and 273 isolates from humans in China, India, Thailand, and Vietnam show that recombination is most likely to occur across spatially and genetically limited distances in natural populations resulting in highly clonal population structure yet sexually reproducing populations. Predicted distributions of three different spatial genetic clusters within P. marneffei overlap with three different bamboo rat host distributions suggesting that recombination within hosts may act to maintain population barriers within P. marneffei.",
author = "Henk, {Daniel A} and R. Shahar-Golan and K.R. Devi and K.J. Boyce and N. Zhan and N.D. Fedorova and W.C. Nierman and P.R. Hsueh and K.Y. Yuen and T.P.M. Sieu and {Van Kinh}, Nguyen and Heiman Wertheim and Baker, {Stephen G.} and Day, {Jeremy N.} and Nongnuch Vanittanakom and Bignell, {Elaine M.} and Alex Andrianopoulos and Fisher, {Matthew C.}",
year = "2012",
month = "10",
day = "4",
doi = "10.1371/journal.ppat.1002851",
language = "English",
volume = "8",
journal = "PLoS Pathogens",
issn = "1553-7366",
publisher = "Public Library of Science (PLOS)",
number = "10",

}

TY - JOUR

T1 - Clonality despite sex: the evolution of host-associated sexual neighborhoods in the pathogenic fungus penicillium marneffei

AU - Henk, Daniel A

AU - Shahar-Golan, R.

AU - Devi, K.R.

AU - Boyce, K.J.

AU - Zhan, N.

AU - Fedorova, N.D.

AU - Nierman, W.C.

AU - Hsueh, P.R.

AU - Yuen, K.Y.

AU - Sieu, T.P.M.

AU - Van Kinh, Nguyen

AU - Wertheim, Heiman

AU - Baker, Stephen G.

AU - Day, Jeremy N.

AU - Vanittanakom, Nongnuch

AU - Bignell, Elaine M.

AU - Andrianopoulos, Alex

AU - Fisher, Matthew C.

PY - 2012/10/4

Y1 - 2012/10/4

N2 - Molecular genetic approaches typically detect recombination in microbes regardless of assumed asexuality. However, genetic data have shown the AIDS-associated pathogen Penicillium marneffei to have extensive spatial genetic structure at local and regional scales, and although there has been some genetic evidence that a sexual cycle is possible, this haploid fungus is thought to be genetically, as well as morphologically, asexual in nature because of its highly clonal population structure. Here we use comparative genomics, experimental mixed-genotype infections, and population genetic data to elucidate the role of recombination in natural populations of P. marneffei. Genome wide comparisons reveal that all the genes required for meiosis are present in P. marneffei, mating type genes are arranged in a similar manner to that found in other heterothallic fungi, and there is evidence of a putatively meiosis-specific mutational process. Experiments suggest that recombination between isolates of compatible mating types may occur during mammal infection. Population genetic data from 34 isolates from bamboo rats in India, Thailand and Vietnam, and 273 isolates from humans in China, India, Thailand, and Vietnam show that recombination is most likely to occur across spatially and genetically limited distances in natural populations resulting in highly clonal population structure yet sexually reproducing populations. Predicted distributions of three different spatial genetic clusters within P. marneffei overlap with three different bamboo rat host distributions suggesting that recombination within hosts may act to maintain population barriers within P. marneffei.

AB - Molecular genetic approaches typically detect recombination in microbes regardless of assumed asexuality. However, genetic data have shown the AIDS-associated pathogen Penicillium marneffei to have extensive spatial genetic structure at local and regional scales, and although there has been some genetic evidence that a sexual cycle is possible, this haploid fungus is thought to be genetically, as well as morphologically, asexual in nature because of its highly clonal population structure. Here we use comparative genomics, experimental mixed-genotype infections, and population genetic data to elucidate the role of recombination in natural populations of P. marneffei. Genome wide comparisons reveal that all the genes required for meiosis are present in P. marneffei, mating type genes are arranged in a similar manner to that found in other heterothallic fungi, and there is evidence of a putatively meiosis-specific mutational process. Experiments suggest that recombination between isolates of compatible mating types may occur during mammal infection. Population genetic data from 34 isolates from bamboo rats in India, Thailand and Vietnam, and 273 isolates from humans in China, India, Thailand, and Vietnam show that recombination is most likely to occur across spatially and genetically limited distances in natural populations resulting in highly clonal population structure yet sexually reproducing populations. Predicted distributions of three different spatial genetic clusters within P. marneffei overlap with three different bamboo rat host distributions suggesting that recombination within hosts may act to maintain population barriers within P. marneffei.

UR - http://www.scopus.com/inward/record.url?scp=84868103431&partnerID=8YFLogxK

UR - http://dx.doi.org/10.1371/journal.ppat.1002851

U2 - 10.1371/journal.ppat.1002851

DO - 10.1371/journal.ppat.1002851

M3 - Article

VL - 8

JO - PLoS Pathogens

JF - PLoS Pathogens

SN - 1553-7366

IS - 10

M1 - e1002851

ER -