Malaria parasites regulate intra-erythrocytic development duration via serpentine receptor 10 to coordinate with host rhythms

Amit Subudhi; Aidan J. O’Donnell; Abhinay Ramaprasad; Hussein M. Abkallo; Abhinav Kaushik; Hifzur Rahman Ansari; Alyaa M. Abdel-Haleem; Fathia Ben Rached; Osamu Kaneko; Richard Culleton; Sarah E. Reece; Arnab Pain

doi:10.1038/s41467-020-16593-y

Malaria parasites regulate intra-erythrocytic development duration via serpentine receptor 10 to coordinate with host rhythms

Amit Subudhi, Aidan J. O’Donnell, Abhinay Ramaprasad, Hussein M. Abkallo, Abhinav Kaushik, Hifzur Rahman Ansari, Alyaa M. Abdel-Haleem, Fathia Ben Rached, Osamu Kaneko, Richard Culleton, Sarah E. Reece, Arnab Pain

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Abstract

Malaria parasites complete their intra-erythrocytic developmental cycle (IDC) in multiples of 24 h suggesting a circadian basis, but the mechanism controlling this periodicity is unknown. Combining in vivo and in vitro approaches utilizing rodent and human malaria parasites, we reveal that: (i) 57% of Plasmodium chabaudi genes exhibit daily rhythms in transcription; (ii) 58% of these genes lose transcriptional rhythmicity when the IDC is out-of-synchrony with host rhythms; (iii) 6% of Plasmodium falciparum genes show 24 h rhythms in expression under free-running conditions; (iv) Serpentine receptor 10 (SR10) has a 24 h transcriptional rhythm and disrupting it in rodent malaria parasites shortens the IDC by 2-3 h; (v) Multiple processes including DNA replication, and the ubiquitin and proteasome pathways, are affected by loss of coordination with host rhythms and by disruption of SR10. Our results reveal malaria parasites are at least partly responsible for scheduling the IDC and coordinating their development with host daily rhythms.

Original language	English (US)
Journal	Nature Communications
Volume	11
Issue number	1
DOIs	https://doi.org/10.1038/s41467-020-16593-y
State	Published - Jun 2 2020

Bibliographical note

KAUST Repository Item: Exported on 2020-10-01
Acknowledged KAUST grant number(s): BAS/1/1020-01-01
Acknowledgements: The project was supported by a faculty baseline fund(BAS/1/1020-01-01) and a Competitive Research Grant (CRG) award from OSR (OSR-2018-CRG6-3392) from the King Abdullah University of Science and Technology (KAUST) to A.P. R.C. is supported by Japanese Society for the Promotion of Science (JSPS), Japan Grant-in-Aid for Scientific Research Nos. 24255009, 25870525, 16K21233, and 19K07526. SER and AJOD are supported by Wellcome (202769/Z/16/Z; 204511/Z/16/Z), the Royal Society (UF110155;NF140517) and the Human Frontier Science Program (RGP0046/2013). The authors thank the staff of the Bioscience Core Laboratory in KAUST for sequencing RNAseq libraries and all members of the Reece lab at the University of Edinburgh and pathogen genomics lab at KAUST for assistance during the experiments. This work was partly conducted at the Joint Usage/Research Center for Tropical Disease, Institute of Tropical Medicine, Nagasaki University, Japan.

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10.1038/s41467-020-16593-y

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Subudhi, A., O’Donnell, A. J., Ramaprasad, A., Abkallo, H. M., Kaushik, A., Ansari, H. R., Abdel-Haleem, A. M., Rached, F. B., Kaneko, O., Culleton, R., Reece, S. E., & Pain, A. (2020). Malaria parasites regulate intra-erythrocytic development duration via serpentine receptor 10 to coordinate with host rhythms. Nature Communications, 11(1). https://doi.org/10.1038/s41467-020-16593-y

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title = "Malaria parasites regulate intra-erythrocytic development duration via serpentine receptor 10 to coordinate with host rhythms",

abstract = "Malaria parasites complete their intra-erythrocytic developmental cycle (IDC) in multiples of 24 h suggesting a circadian basis, but the mechanism controlling this periodicity is unknown. Combining in vivo and in vitro approaches utilizing rodent and human malaria parasites, we reveal that: (i) 57% of Plasmodium chabaudi genes exhibit daily rhythms in transcription; (ii) 58% of these genes lose transcriptional rhythmicity when the IDC is out-of-synchrony with host rhythms; (iii) 6% of Plasmodium falciparum genes show 24 h rhythms in expression under free-running conditions; (iv) Serpentine receptor 10 (SR10) has a 24 h transcriptional rhythm and disrupting it in rodent malaria parasites shortens the IDC by 2-3 h; (v) Multiple processes including DNA replication, and the ubiquitin and proteasome pathways, are affected by loss of coordination with host rhythms and by disruption of SR10. Our results reveal malaria parasites are at least partly responsible for scheduling the IDC and coordinating their development with host daily rhythms.",

author = "Amit Subudhi and O{\textquoteright}Donnell, {Aidan J.} and Abhinay Ramaprasad and Abkallo, {Hussein M.} and Abhinav Kaushik and Ansari, {Hifzur Rahman} and Abdel-Haleem, {Alyaa M.} and Rached, {Fathia Ben} and Osamu Kaneko and Richard Culleton and Reece, {Sarah E.} and Arnab Pain",

note = "KAUST Repository Item: Exported on 2020-10-01 Acknowledged KAUST grant number(s): BAS/1/1020-01-01 Acknowledgements: The project was supported by a faculty baseline fund(BAS/1/1020-01-01) and a Competitive Research Grant (CRG) award from OSR (OSR-2018-CRG6-3392) from the King Abdullah University of Science and Technology (KAUST) to A.P. R.C. is supported by Japanese Society for the Promotion of Science (JSPS), Japan Grant-in-Aid for Scientific Research Nos. 24255009, 25870525, 16K21233, and 19K07526. SER and AJOD are supported by Wellcome (202769/Z/16/Z; 204511/Z/16/Z), the Royal Society (UF110155;NF140517) and the Human Frontier Science Program (RGP0046/2013). The authors thank the staff of the Bioscience Core Laboratory in KAUST for sequencing RNAseq libraries and all members of the Reece lab at the University of Edinburgh and pathogen genomics lab at KAUST for assistance during the experiments. This work was partly conducted at the Joint Usage/Research Center for Tropical Disease, Institute of Tropical Medicine, Nagasaki University, Japan.",

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Subudhi, A, O’Donnell, AJ, Ramaprasad, A, Abkallo, HM, Kaushik, A, Ansari, HR, Abdel-Haleem, AM, Rached, FB, Kaneko, O, Culleton, R, Reece, SE & Pain, A 2020, 'Malaria parasites regulate intra-erythrocytic development duration via serpentine receptor 10 to coordinate with host rhythms', Nature Communications, vol. 11, no. 1. https://doi.org/10.1038/s41467-020-16593-y

TY - JOUR

T1 - Malaria parasites regulate intra-erythrocytic development duration via serpentine receptor 10 to coordinate with host rhythms

AU - Subudhi, Amit

AU - O’Donnell, Aidan J.

AU - Ramaprasad, Abhinay

AU - Abkallo, Hussein M.

AU - Kaushik, Abhinav

AU - Ansari, Hifzur Rahman

AU - Abdel-Haleem, Alyaa M.

AU - Rached, Fathia Ben

AU - Kaneko, Osamu

AU - Culleton, Richard

AU - Reece, Sarah E.

AU - Pain, Arnab

N1 - KAUST Repository Item: Exported on 2020-10-01 Acknowledged KAUST grant number(s): BAS/1/1020-01-01 Acknowledgements: The project was supported by a faculty baseline fund(BAS/1/1020-01-01) and a Competitive Research Grant (CRG) award from OSR (OSR-2018-CRG6-3392) from the King Abdullah University of Science and Technology (KAUST) to A.P. R.C. is supported by Japanese Society for the Promotion of Science (JSPS), Japan Grant-in-Aid for Scientific Research Nos. 24255009, 25870525, 16K21233, and 19K07526. SER and AJOD are supported by Wellcome (202769/Z/16/Z; 204511/Z/16/Z), the Royal Society (UF110155;NF140517) and the Human Frontier Science Program (RGP0046/2013). The authors thank the staff of the Bioscience Core Laboratory in KAUST for sequencing RNAseq libraries and all members of the Reece lab at the University of Edinburgh and pathogen genomics lab at KAUST for assistance during the experiments. This work was partly conducted at the Joint Usage/Research Center for Tropical Disease, Institute of Tropical Medicine, Nagasaki University, Japan.

PY - 2020/6/2

Y1 - 2020/6/2

N2 - Malaria parasites complete their intra-erythrocytic developmental cycle (IDC) in multiples of 24 h suggesting a circadian basis, but the mechanism controlling this periodicity is unknown. Combining in vivo and in vitro approaches utilizing rodent and human malaria parasites, we reveal that: (i) 57% of Plasmodium chabaudi genes exhibit daily rhythms in transcription; (ii) 58% of these genes lose transcriptional rhythmicity when the IDC is out-of-synchrony with host rhythms; (iii) 6% of Plasmodium falciparum genes show 24 h rhythms in expression under free-running conditions; (iv) Serpentine receptor 10 (SR10) has a 24 h transcriptional rhythm and disrupting it in rodent malaria parasites shortens the IDC by 2-3 h; (v) Multiple processes including DNA replication, and the ubiquitin and proteasome pathways, are affected by loss of coordination with host rhythms and by disruption of SR10. Our results reveal malaria parasites are at least partly responsible for scheduling the IDC and coordinating their development with host daily rhythms.

AB - Malaria parasites complete their intra-erythrocytic developmental cycle (IDC) in multiples of 24 h suggesting a circadian basis, but the mechanism controlling this periodicity is unknown. Combining in vivo and in vitro approaches utilizing rodent and human malaria parasites, we reveal that: (i) 57% of Plasmodium chabaudi genes exhibit daily rhythms in transcription; (ii) 58% of these genes lose transcriptional rhythmicity when the IDC is out-of-synchrony with host rhythms; (iii) 6% of Plasmodium falciparum genes show 24 h rhythms in expression under free-running conditions; (iv) Serpentine receptor 10 (SR10) has a 24 h transcriptional rhythm and disrupting it in rodent malaria parasites shortens the IDC by 2-3 h; (v) Multiple processes including DNA replication, and the ubiquitin and proteasome pathways, are affected by loss of coordination with host rhythms and by disruption of SR10. Our results reveal malaria parasites are at least partly responsible for scheduling the IDC and coordinating their development with host daily rhythms.

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UR - http://www.nature.com/articles/s41467-020-16593-y

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U2 - 10.1038/s41467-020-16593-y

DO - 10.1038/s41467-020-16593-y

M3 - Article

C2 - 32488076

SN - 2041-1723

VL - 11

JO - Nature Communications

JF - Nature Communications

IS - 1

ER -

Malaria parasites regulate intra-erythrocytic development duration via serpentine receptor 10 to coordinate with host rhythms

Abstract

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