Chromerid genomes reveal the evolutionary path from photosynthetic algae to obligate intracellular parasites

Yong Woo; Hifzur Rahman Ansari; Thomas D. Otto; Christen M K Linger; Martin K. Olisko; Jan Michálek; Alka Saxena; Dhanasekaran Shanmugam; Annageldi Tayyrov; Alaguraj Veluchamy; Shahjahan Ali; Axel Bernal; Javier Del Campo; Jaromír Cihlář; Pavel Flegontov; Sebastian G. Gornik; Eva Hajdušková; Aleš Horák; Jan Janouškovec; Nicholas J. Katris; Fred D. Mast; Diego Miranda-Saavedra; Tobias Mourier; Raeece Naeem; Mridul Nair; Aswini Kumar Panigrahi; Neil D. Rawlings; Eriko Padron Regalado; Abhinay Ramaprasad; Nadira Samad; Aleš Tomčala; Jon Wilkes; Daniel E. Neafsey; Christian Doerig; Chris Bowler; Patrick J. Keeling; David S. Roos; Joel B. Dacks; Thomas J. Templeton; Ross F. Waller; Julius Lukeš; Miroslav Oborník; Arnab Pain

doi:10.7554/eLife.06974

Chromerid genomes reveal the evolutionary path from photosynthetic algae to obligate intracellular parasites

Yong Woo, Hifzur Rahman Ansari, Thomas D. Otto, Christen M K Linger, Martin K. Olisko, Jan Michálek, Alka Saxena, Dhanasekaran Shanmugam, Annageldi Tayyrov, Alaguraj Veluchamy, Shahjahan Ali, Axel Bernal, Javier Del Campo, Jaromír Cihlář, Pavel Flegontov, Sebastian G. Gornik, Eva Hajdušková, Aleš Horák, Jan Janouškovec, Nicholas J. KatrisFred D. Mast, Diego Miranda-Saavedra, Tobias Mourier, Raeece Naeem, Mridul Nair, Aswini Kumar Panigrahi, Neil D. Rawlings, Eriko Padron Regalado, Abhinay Ramaprasad, Nadira Samad, Aleš Tomčala, Jon Wilkes, Daniel E. Neafsey, Christian Doerig, Chris Bowler, Patrick J. Keeling, David S. Roos, Joel B. Dacks, Thomas J. Templeton, Ross F. Waller, Julius Lukeš, Miroslav Oborník, Arnab Pain

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Abstract

The eukaryotic phylum Apicomplexa encompasses thousands of obligate intracellular parasites of humans and animals with immense socio-economic and health impacts. We sequenced nuclear genomes of Chromera velia and Vitrella brassicaformis, free-living non-parasitic photosynthetic algae closely related to apicomplexans. Proteins from key metabolic pathways and from the endomembrane trafficking systems associated with a free-living lifestyle have been progressively and non-randomly lost during adaptation to parasitism. The free-living ancestor contained a broad repertoire of genes many of which were repurposed for parasitic processes, such as extracellular proteins, components of a motility apparatus, and DNA- and RNA-binding protein families. Based on transcriptome analyses across 36 environmental conditions, Chromera orthologs of apicomplexan invasion-related motility genes were co-regulated with genes encoding the flagellar apparatus, supporting the functional contribution of flagella to the evolution of invasion machinery. This study provides insights into how obligate parasites with diverse life strategies arose from a once free-living phototrophic marine alga. © Woo et al.

Original language	English (US)
Pages (from-to)	1-41
Number of pages	41
Journal	eLife
Volume	4
Issue number	JULY 2015
DOIs	https://doi.org/10.7554/eLife.06974
State	Published - Jul 15 2015

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KAUST Repository Item: Exported on 2020-10-01

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10.7554/eLife.06974

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Woo, Y., Ansari, H. R., Otto, T. D., Linger, C. M. K., Olisko, M. K., Michálek, J., Saxena, A., Shanmugam, D., Tayyrov, A., Veluchamy, A., Ali, S., Bernal, A., Del Campo, J., Cihlář, J., Flegontov, P., Gornik, S. G., Hajdušková, E., Horák, A., Janouškovec, J., ... Pain, A. (2015). Chromerid genomes reveal the evolutionary path from photosynthetic algae to obligate intracellular parasites. eLife, 4(JULY 2015), 1-41. https://doi.org/10.7554/eLife.06974

@article{407c2a83871349049d610fac5ee7ada9,

title = "Chromerid genomes reveal the evolutionary path from photosynthetic algae to obligate intracellular parasites",

abstract = "The eukaryotic phylum Apicomplexa encompasses thousands of obligate intracellular parasites of humans and animals with immense socio-economic and health impacts. We sequenced nuclear genomes of Chromera velia and Vitrella brassicaformis, free-living non-parasitic photosynthetic algae closely related to apicomplexans. Proteins from key metabolic pathways and from the endomembrane trafficking systems associated with a free-living lifestyle have been progressively and non-randomly lost during adaptation to parasitism. The free-living ancestor contained a broad repertoire of genes many of which were repurposed for parasitic processes, such as extracellular proteins, components of a motility apparatus, and DNA- and RNA-binding protein families. Based on transcriptome analyses across 36 environmental conditions, Chromera orthologs of apicomplexan invasion-related motility genes were co-regulated with genes encoding the flagellar apparatus, supporting the functional contribution of flagella to the evolution of invasion machinery. This study provides insights into how obligate parasites with diverse life strategies arose from a once free-living phototrophic marine alga. {\textcopyright} Woo et al.",

author = "Yong Woo and Ansari, {Hifzur Rahman} and Otto, {Thomas D.} and Linger, {Christen M K} and Olisko, {Martin K.} and Jan Mich{\'a}lek and Alka Saxena and Dhanasekaran Shanmugam and Annageldi Tayyrov and Alaguraj Veluchamy and Shahjahan Ali and Axel Bernal and {Del Campo}, Javier and Jarom{\'i}r Cihl{\'a}{\v r} and Pavel Flegontov and Gornik, {Sebastian G.} and Eva Hajdu{\v s}kov{\'a} and Ale{\v s} Hor{\'a}k and Jan Janou{\v s}kovec and Katris, {Nicholas J.} and Mast, {Fred D.} and Diego Miranda-Saavedra and Tobias Mourier and Raeece Naeem and Mridul Nair and Panigrahi, {Aswini Kumar} and Rawlings, {Neil D.} and {Padron Regalado}, Eriko and Abhinay Ramaprasad and Nadira Samad and Ale{\v s} Tom{\v c}ala and Jon Wilkes and Neafsey, {Daniel E.} and Christian Doerig and Chris Bowler and Keeling, {Patrick J.} and Roos, {David S.} and Dacks, {Joel B.} and Templeton, {Thomas J.} and Waller, {Ross F.} and Julius Luke{\v s} and Miroslav Oborn{\'i}k and Arnab Pain",

note = "KAUST Repository Item: Exported on 2020-10-01",

year = "2015",

month = jul,

day = "15",

doi = "10.7554/eLife.06974",

language = "English (US)",

volume = "4",

pages = "1--41",

journal = "eLife",

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Woo, Y, Ansari, HR, Otto, TD, Linger, CMK, Olisko, MK, Michálek, J, Saxena, A, Shanmugam, D, Tayyrov, A, Veluchamy, A, Ali, S, Bernal, A, Del Campo, J, Cihlář, J, Flegontov, P, Gornik, SG, Hajdušková, E, Horák, A, Janouškovec, J, Katris, NJ, Mast, FD, Miranda-Saavedra, D, Mourier, T, Naeem, R, Nair, M, Panigrahi, AK, Rawlings, ND, Padron Regalado, E, Ramaprasad, A, Samad, N, Tomčala, A, Wilkes, J, Neafsey, DE, Doerig, C, Bowler, C, Keeling, PJ, Roos, DS, Dacks, JB, Templeton, TJ, Waller, RF, Lukeš, J, Oborník, M & Pain, A 2015, 'Chromerid genomes reveal the evolutionary path from photosynthetic algae to obligate intracellular parasites', eLife, vol. 4, no. JULY 2015, pp. 1-41. https://doi.org/10.7554/eLife.06974

TY - JOUR

T1 - Chromerid genomes reveal the evolutionary path from photosynthetic algae to obligate intracellular parasites

AU - Woo, Yong

AU - Ansari, Hifzur Rahman

AU - Otto, Thomas D.

AU - Linger, Christen M K

AU - Olisko, Martin K.

AU - Michálek, Jan

AU - Saxena, Alka

AU - Shanmugam, Dhanasekaran

AU - Tayyrov, Annageldi

AU - Veluchamy, Alaguraj

AU - Ali, Shahjahan

AU - Bernal, Axel

AU - Del Campo, Javier

AU - Cihlář, Jaromír

AU - Flegontov, Pavel

AU - Gornik, Sebastian G.

AU - Hajdušková, Eva

AU - Horák, Aleš

AU - Janouškovec, Jan

AU - Katris, Nicholas J.

AU - Mast, Fred D.

AU - Miranda-Saavedra, Diego

AU - Mourier, Tobias

AU - Naeem, Raeece

AU - Nair, Mridul

AU - Panigrahi, Aswini Kumar

AU - Rawlings, Neil D.

AU - Padron Regalado, Eriko

AU - Ramaprasad, Abhinay

AU - Samad, Nadira

AU - Tomčala, Aleš

AU - Wilkes, Jon

AU - Neafsey, Daniel E.

AU - Doerig, Christian

AU - Bowler, Chris

AU - Keeling, Patrick J.

AU - Roos, David S.

AU - Dacks, Joel B.

AU - Templeton, Thomas J.

AU - Waller, Ross F.

AU - Lukeš, Julius

AU - Oborník, Miroslav

AU - Pain, Arnab

N1 - KAUST Repository Item: Exported on 2020-10-01

PY - 2015/7/15

Y1 - 2015/7/15

N2 - The eukaryotic phylum Apicomplexa encompasses thousands of obligate intracellular parasites of humans and animals with immense socio-economic and health impacts. We sequenced nuclear genomes of Chromera velia and Vitrella brassicaformis, free-living non-parasitic photosynthetic algae closely related to apicomplexans. Proteins from key metabolic pathways and from the endomembrane trafficking systems associated with a free-living lifestyle have been progressively and non-randomly lost during adaptation to parasitism. The free-living ancestor contained a broad repertoire of genes many of which were repurposed for parasitic processes, such as extracellular proteins, components of a motility apparatus, and DNA- and RNA-binding protein families. Based on transcriptome analyses across 36 environmental conditions, Chromera orthologs of apicomplexan invasion-related motility genes were co-regulated with genes encoding the flagellar apparatus, supporting the functional contribution of flagella to the evolution of invasion machinery. This study provides insights into how obligate parasites with diverse life strategies arose from a once free-living phototrophic marine alga. © Woo et al.

AB - The eukaryotic phylum Apicomplexa encompasses thousands of obligate intracellular parasites of humans and animals with immense socio-economic and health impacts. We sequenced nuclear genomes of Chromera velia and Vitrella brassicaformis, free-living non-parasitic photosynthetic algae closely related to apicomplexans. Proteins from key metabolic pathways and from the endomembrane trafficking systems associated with a free-living lifestyle have been progressively and non-randomly lost during adaptation to parasitism. The free-living ancestor contained a broad repertoire of genes many of which were repurposed for parasitic processes, such as extracellular proteins, components of a motility apparatus, and DNA- and RNA-binding protein families. Based on transcriptome analyses across 36 environmental conditions, Chromera orthologs of apicomplexan invasion-related motility genes were co-regulated with genes encoding the flagellar apparatus, supporting the functional contribution of flagella to the evolution of invasion machinery. This study provides insights into how obligate parasites with diverse life strategies arose from a once free-living phototrophic marine alga. © Woo et al.

UR - http://hdl.handle.net/10754/565962

UR - https://elifesciences.org/articles/06974

UR - http://www.scopus.com/inward/record.url?scp=84937408158&partnerID=8YFLogxK

U2 - 10.7554/eLife.06974

DO - 10.7554/eLife.06974

M3 - Article

C2 - 26175406

SN - 2050-084X

VL - 4

SP - 1

EP - 41

JO - eLife

JF - eLife

IS - JULY 2015

ER -

Chromerid genomes reveal the evolutionary path from photosynthetic algae to obligate intracellular parasites

Abstract

Bibliographical note

UN SDGs

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