Leishmania genome dynamics during environmental adaptation reveals strain-specific differences in gene copy number variation, karyotype instability, and telomeric amplification

Giovanni Bussotti; Evi Gouzelou; Mariana Cortes Boite; Ihcen Kherachi; Zoubir Harrat; Naouel Eddaikra; Jeremy Charles Mottram; Maria Antoniou; Vasiliki Christodoulou; Aymen Bali; Fatma Z. Guerfali; Dhafer Laouini; Maowla Mukhtar; Franck Dumetz; Jean-Claude Dujardin; Despina Smirlis; Pierre Lechat; Pascale Pescher; Adil El Hamouchi; Meryem Lemrani; Carmen Chicharro; Ivonne Pamela Llanes-Acevedo; Laura Botana; Israel Cruz; Javier Moreno; Fakhri Jeddi; Karim Aoun; Aida Bouratbine; Elisa Cupolillo; Gerald F. Spath

doi:10.1128/mBio.01399-18

Leishmania genome dynamics during environmental adaptation reveals strain-specific differences in gene copy number variation, karyotype instability, and telomeric amplification

Giovanni Bussotti, Evi Gouzelou, Mariana Cortes Boite, Ihcen Kherachi, Zoubir Harrat, Naouel Eddaikra, Jeremy Charles Mottram, Maria Antoniou, Vasiliki Christodoulou, Aymen Bali, Fatma Z. Guerfali, Dhafer Laouini, Maowla Mukhtar, Franck Dumetz, Jean-Claude Dujardin, Despina Smirlis, Pierre Lechat, Pascale Pescher, Adil El Hamouchi, Meryem LemraniCarmen Chicharro, Ivonne Pamela Llanes-Acevedo, Laura Botana, Israel Cruz, Javier Moreno, Fakhri Jeddi, Karim Aoun, Aida Bouratbine, Elisa Cupolillo, Gerald F. Spath

Biology

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Abstract

Protozoan parasites of the genus Leishmania adapt to environmental change through chromosome and gene copy number variations. Only little is known on external or intrinsic factors that govern Leishmania genomic adaptation. Here, by conducting longitudinal genome analyses of ten new Leishmania clinical isolates, we uncovered important differences in gene copy number among genetically highly related strains and revealed gain and loss of gene copies as potential drivers of long-term environmental adaptation in the field. In contrast, chromosome rather than gene amplification was associated with short-term environmental adaptation to in vitro culture. Karyotypic solutions were highly reproducible but unique for a given strain, suggesting that chromosome amplification is under positive selection and dependent on species- and strain-specific, intrinsic factors. We revealed a progressive increase in read depth towards the chromosome ends for various Leishmania isolates, which may represent a non-classical mechanism of telomere maintenance that can preserve integrity of chromosome ends during selection for fast in vitro growth. Together our data draw a complex picture of Leishmania genomic adaptation in the field and in culture, which is driven by a combination of intrinsic genetic factors that generate strain-specific, phenotypic variations, which are under environmental selection and allow for fitness gain.

Original language	English
Article number	e01399-18
Number of pages	18
Journal	MBio
Volume	9
Issue number	6
DOIs	https://doi.org/10.1128/mBio.01399-18
Publication status	Published - 6 Nov 2018

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10.1128/mBio.01399-18

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© 2018 Bussotti et al.
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Jeremy Charles Mottram
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Bussotti, G., Gouzelou, E., Cortes Boite, M., Kherachi, I., Harrat, Z., Eddaikra, N., Mottram, J. C., Antoniou, M., Christodoulou, V., Bali, A., Guerfali, F. Z., Laouini, D., Mukhtar, M., Dumetz, F., Dujardin, J-C., Smirlis, D., Lechat, P., Pescher, P., El Hamouchi, A., ... Spath, G. F. (2018). Leishmania genome dynamics during environmental adaptation reveals strain-specific differences in gene copy number variation, karyotype instability, and telomeric amplification. MBio, 9(6), [ e01399-18]. https://doi.org/10.1128/mBio.01399-18

@article{4a351df8cf5647509fe383f016a3cd63,

title = "Leishmania genome dynamics during environmental adaptation reveals strain-specific differences in gene copy number variation, karyotype instability, and telomeric amplification",

abstract = "Protozoan parasites of the genus Leishmania adapt to environmental change through chromosome and gene copy number variations. Only little is known on external or intrinsic factors that govern Leishmania genomic adaptation. Here, by conducting longitudinal genome analyses of ten new Leishmania clinical isolates, we uncovered important differences in gene copy number among genetically highly related strains and revealed gain and loss of gene copies as potential drivers of long-term environmental adaptation in the field. In contrast, chromosome rather than gene amplification was associated with short-term environmental adaptation to in vitro culture. Karyotypic solutions were highly reproducible but unique for a given strain, suggesting that chromosome amplification is under positive selection and dependent on species- and strain-specific, intrinsic factors. We revealed a progressive increase in read depth towards the chromosome ends for various Leishmania isolates, which may represent a non-classical mechanism of telomere maintenance that can preserve integrity of chromosome ends during selection for fast in vitro growth. Together our data draw a complex picture of Leishmania genomic adaptation in the field and in culture, which is driven by a combination of intrinsic genetic factors that generate strain-specific, phenotypic variations, which are under environmental selection and allow for fitness gain.",

author = "Giovanni Bussotti and Evi Gouzelou and {Cortes Boite}, Mariana and Ihcen Kherachi and Zoubir Harrat and Naouel Eddaikra and Mottram, {Jeremy Charles} and Maria Antoniou and Vasiliki Christodoulou and Aymen Bali and Guerfali, {Fatma Z.} and Dhafer Laouini and Maowla Mukhtar and Franck Dumetz and Jean-Claude Dujardin and Despina Smirlis and Pierre Lechat and Pascale Pescher and {El Hamouchi}, Adil and Meryem Lemrani and Carmen Chicharro and Llanes-Acevedo, {Ivonne Pamela} and Laura Botana and Israel Cruz and Javier Moreno and Fakhri Jeddi and Karim Aoun and Aida Bouratbine and Elisa Cupolillo and Spath, {Gerald F.}",

note = "{\textcopyright} 2018 Bussotti et al.",

year = "2018",

month = nov,

day = "6",

doi = "10.1128/mBio.01399-18",

language = "English",

volume = "9",

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Bussotti, G, Gouzelou, E, Cortes Boite, M, Kherachi, I, Harrat, Z, Eddaikra, N, Mottram, JC, Antoniou, M, Christodoulou, V, Bali, A, Guerfali, FZ, Laouini, D, Mukhtar, M, Dumetz, F, Dujardin, J-C, Smirlis, D, Lechat, P, Pescher, P, El Hamouchi, A, Lemrani, M, Chicharro, C, Llanes-Acevedo, IP, Botana, L, Cruz, I, Moreno, J, Jeddi, F, Aoun, K, Bouratbine, A, Cupolillo, E & Spath, GF 2018, 'Leishmania genome dynamics during environmental adaptation reveals strain-specific differences in gene copy number variation, karyotype instability, and telomeric amplification', MBio, vol. 9, no. 6, e01399-18. https://doi.org/10.1128/mBio.01399-18

TY - JOUR

T1 - Leishmania genome dynamics during environmental adaptation reveals strain-specific differences in gene copy number variation, karyotype instability, and telomeric amplification

AU - Bussotti, Giovanni

AU - Gouzelou, Evi

AU - Cortes Boite, Mariana

AU - Kherachi, Ihcen

AU - Harrat, Zoubir

AU - Eddaikra, Naouel

AU - Mottram, Jeremy Charles

AU - Antoniou, Maria

AU - Christodoulou, Vasiliki

AU - Bali, Aymen

AU - Guerfali, Fatma Z.

AU - Laouini, Dhafer

AU - Mukhtar, Maowla

AU - Dumetz, Franck

AU - Dujardin, Jean-Claude

AU - Smirlis, Despina

AU - Lechat, Pierre

AU - Pescher, Pascale

AU - El Hamouchi, Adil

AU - Lemrani, Meryem

AU - Chicharro, Carmen

AU - Llanes-Acevedo, Ivonne Pamela

AU - Botana, Laura

AU - Cruz, Israel

AU - Moreno, Javier

AU - Jeddi, Fakhri

AU - Aoun, Karim

AU - Bouratbine, Aida

AU - Cupolillo, Elisa

AU - Spath, Gerald F.

PY - 2018/11/6

Y1 - 2018/11/6

N2 - Protozoan parasites of the genus Leishmania adapt to environmental change through chromosome and gene copy number variations. Only little is known on external or intrinsic factors that govern Leishmania genomic adaptation. Here, by conducting longitudinal genome analyses of ten new Leishmania clinical isolates, we uncovered important differences in gene copy number among genetically highly related strains and revealed gain and loss of gene copies as potential drivers of long-term environmental adaptation in the field. In contrast, chromosome rather than gene amplification was associated with short-term environmental adaptation to in vitro culture. Karyotypic solutions were highly reproducible but unique for a given strain, suggesting that chromosome amplification is under positive selection and dependent on species- and strain-specific, intrinsic factors. We revealed a progressive increase in read depth towards the chromosome ends for various Leishmania isolates, which may represent a non-classical mechanism of telomere maintenance that can preserve integrity of chromosome ends during selection for fast in vitro growth. Together our data draw a complex picture of Leishmania genomic adaptation in the field and in culture, which is driven by a combination of intrinsic genetic factors that generate strain-specific, phenotypic variations, which are under environmental selection and allow for fitness gain.

AB - Protozoan parasites of the genus Leishmania adapt to environmental change through chromosome and gene copy number variations. Only little is known on external or intrinsic factors that govern Leishmania genomic adaptation. Here, by conducting longitudinal genome analyses of ten new Leishmania clinical isolates, we uncovered important differences in gene copy number among genetically highly related strains and revealed gain and loss of gene copies as potential drivers of long-term environmental adaptation in the field. In contrast, chromosome rather than gene amplification was associated with short-term environmental adaptation to in vitro culture. Karyotypic solutions were highly reproducible but unique for a given strain, suggesting that chromosome amplification is under positive selection and dependent on species- and strain-specific, intrinsic factors. We revealed a progressive increase in read depth towards the chromosome ends for various Leishmania isolates, which may represent a non-classical mechanism of telomere maintenance that can preserve integrity of chromosome ends during selection for fast in vitro growth. Together our data draw a complex picture of Leishmania genomic adaptation in the field and in culture, which is driven by a combination of intrinsic genetic factors that generate strain-specific, phenotypic variations, which are under environmental selection and allow for fitness gain.

U2 - 10.1128/mBio.01399-18

DO - 10.1128/mBio.01399-18

M3 - Article

SN - 2161-2129

VL - 9

JO - MBio

JF - MBio

IS - 6

M1 - e01399-18

ER -

Leishmania genome dynamics during environmental adaptation reveals strain-specific differences in gene copy number variation, karyotype instability, and telomeric amplification

Abstract

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