Enzymes of type II fatty acid synthesis and apicoplast differentiation and division in eimeria tenella

D.J.P. Ferguson, S.A. Campbell, F.L. Henriquez, L. Phan, E. Mui, T.A. Richards, S.P. Muench, M. Allary, J.Z. Lu, S.T. Prigge, F. Tomley, M.W. Shirley, D.W. Rice, R. McLeod, C.W. Roberts

Research output: Contribution to journalArticle

32 Citations (Scopus)

Abstract

Apicomplexan parasites, Eimeria tenella, Plasmodium spp. and Toxoplasma gondii, possess a homologous plastid-like organelle termed the apicoplast, derived from the endosymbiotic enslavement of a photosynthetic alga. However, currently no eimerian nuclear encoded apicoplast targeted proteins have been identified, unlike in Plasmodium spp. and T. gondii. In this study, we demonstrate that nuclear encoded enoyl reductase of E. tenella (EtENR) has a predicted N-terminal bipartite transit sequence, typical of apicoplast-targeted proteins. Using a combination of immunocytochemistry and EM we demonstrate that this fatty acid biosynthesis protein is located in the apicoplast of E. tenella. Using the EtENR as a tool to mark apicoplast development during the Eimeria lifecycle, we demonstrate that nuclear and apicoplast division appear to be independent events, both organelles dividing prior to daughter cell formation, with each daughter cell possessing one to four apicoplasts. We believe this is the first report of multiple apicoplasts present in the infectious stage of an apicomplexan parasite. Furthermore, the microgametes lacked an identifiable apicoplast consistent with maternal inheritance via the macrogamete. It was found that the size of the organelle and the abundance of EtENR varied with developmental stage of the E. tenella lifecycle. The high levels of EtENR protein observed during asexual development and macrogametogony is potentially associated with the increased synthesis of fatty acids required for the rapid formation of numerous merozoites and for the extracellular development and survival of the oocyst. Taken together the data demonstrate that the E. tenella apicoplast participates in type II fatty acid biosynthesis with increased expression of ENR during parasite growth. Apicoplast division results in the simultaneous formation of multiple fragments. The division mechanism is unknown, but is independent of nuclear division and occurs prior to daughter formation.
LanguageEnglish
Pages33-51
Number of pages18
JournalInternational Journal for Parasitology
Volume37
Issue number1
DOIs
Publication statusPublished - 2007

Fingerprint

Apicoplasts
Eimeria tenella
Fatty Acids
Enzymes
Cell Nucleus Division
Parasites
Plasmodium
Toxoplasma
Organelles
Organelle Size
Slavery
Eimeria
Merozoites
Proteins
Plastids
Oocysts
Protein Biosynthesis

Keywords

  • Eimeria tenella
  • apicoplast
  • enoyl reductase
  • immunocytochemistry
  • stage specific expression

Cite this

Ferguson, D.J.P. ; Campbell, S.A. ; Henriquez, F.L. ; Phan, L. ; Mui, E. ; Richards, T.A. ; Muench, S.P. ; Allary, M. ; Lu, J.Z. ; Prigge, S.T. ; Tomley, F. ; Shirley, M.W. ; Rice, D.W. ; McLeod, R. ; Roberts, C.W. / Enzymes of type II fatty acid synthesis and apicoplast differentiation and division in eimeria tenella. In: International Journal for Parasitology. 2007 ; Vol. 37, No. 1. pp. 33-51.
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Ferguson, DJP, Campbell, SA, Henriquez, FL, Phan, L, Mui, E, Richards, TA, Muench, SP, Allary, M, Lu, JZ, Prigge, ST, Tomley, F, Shirley, MW, Rice, DW, McLeod, R & Roberts, CW 2007, 'Enzymes of type II fatty acid synthesis and apicoplast differentiation and division in eimeria tenella' International Journal for Parasitology, vol. 37, no. 1, pp. 33-51. https://doi.org/10.1016/j.ijpara.2006.10.003

Enzymes of type II fatty acid synthesis and apicoplast differentiation and division in eimeria tenella. / Ferguson, D.J.P.; Campbell, S.A.; Henriquez, F.L.; Phan, L.; Mui, E.; Richards, T.A.; Muench, S.P.; Allary, M.; Lu, J.Z.; Prigge, S.T.; Tomley, F.; Shirley, M.W.; Rice, D.W.; McLeod, R.; Roberts, C.W.

In: International Journal for Parasitology, Vol. 37, No. 1, 2007, p. 33-51.

Research output: Contribution to journalArticle

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T1 - Enzymes of type II fatty acid synthesis and apicoplast differentiation and division in eimeria tenella

AU - Ferguson, D.J.P.

AU - Campbell, S.A.

AU - Henriquez, F.L.

AU - Phan, L.

AU - Mui, E.

AU - Richards, T.A.

AU - Muench, S.P.

AU - Allary, M.

AU - Lu, J.Z.

AU - Prigge, S.T.

AU - Tomley, F.

AU - Shirley, M.W.

AU - Rice, D.W.

AU - McLeod, R.

AU - Roberts, C.W.

PY - 2007

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N2 - Apicomplexan parasites, Eimeria tenella, Plasmodium spp. and Toxoplasma gondii, possess a homologous plastid-like organelle termed the apicoplast, derived from the endosymbiotic enslavement of a photosynthetic alga. However, currently no eimerian nuclear encoded apicoplast targeted proteins have been identified, unlike in Plasmodium spp. and T. gondii. In this study, we demonstrate that nuclear encoded enoyl reductase of E. tenella (EtENR) has a predicted N-terminal bipartite transit sequence, typical of apicoplast-targeted proteins. Using a combination of immunocytochemistry and EM we demonstrate that this fatty acid biosynthesis protein is located in the apicoplast of E. tenella. Using the EtENR as a tool to mark apicoplast development during the Eimeria lifecycle, we demonstrate that nuclear and apicoplast division appear to be independent events, both organelles dividing prior to daughter cell formation, with each daughter cell possessing one to four apicoplasts. We believe this is the first report of multiple apicoplasts present in the infectious stage of an apicomplexan parasite. Furthermore, the microgametes lacked an identifiable apicoplast consistent with maternal inheritance via the macrogamete. It was found that the size of the organelle and the abundance of EtENR varied with developmental stage of the E. tenella lifecycle. The high levels of EtENR protein observed during asexual development and macrogametogony is potentially associated with the increased synthesis of fatty acids required for the rapid formation of numerous merozoites and for the extracellular development and survival of the oocyst. Taken together the data demonstrate that the E. tenella apicoplast participates in type II fatty acid biosynthesis with increased expression of ENR during parasite growth. Apicoplast division results in the simultaneous formation of multiple fragments. The division mechanism is unknown, but is independent of nuclear division and occurs prior to daughter formation.

AB - Apicomplexan parasites, Eimeria tenella, Plasmodium spp. and Toxoplasma gondii, possess a homologous plastid-like organelle termed the apicoplast, derived from the endosymbiotic enslavement of a photosynthetic alga. However, currently no eimerian nuclear encoded apicoplast targeted proteins have been identified, unlike in Plasmodium spp. and T. gondii. In this study, we demonstrate that nuclear encoded enoyl reductase of E. tenella (EtENR) has a predicted N-terminal bipartite transit sequence, typical of apicoplast-targeted proteins. Using a combination of immunocytochemistry and EM we demonstrate that this fatty acid biosynthesis protein is located in the apicoplast of E. tenella. Using the EtENR as a tool to mark apicoplast development during the Eimeria lifecycle, we demonstrate that nuclear and apicoplast division appear to be independent events, both organelles dividing prior to daughter cell formation, with each daughter cell possessing one to four apicoplasts. We believe this is the first report of multiple apicoplasts present in the infectious stage of an apicomplexan parasite. Furthermore, the microgametes lacked an identifiable apicoplast consistent with maternal inheritance via the macrogamete. It was found that the size of the organelle and the abundance of EtENR varied with developmental stage of the E. tenella lifecycle. The high levels of EtENR protein observed during asexual development and macrogametogony is potentially associated with the increased synthesis of fatty acids required for the rapid formation of numerous merozoites and for the extracellular development and survival of the oocyst. Taken together the data demonstrate that the E. tenella apicoplast participates in type II fatty acid biosynthesis with increased expression of ENR during parasite growth. Apicoplast division results in the simultaneous formation of multiple fragments. The division mechanism is unknown, but is independent of nuclear division and occurs prior to daughter formation.

KW - Eimeria tenella

KW - apicoplast

KW - enoyl reductase

KW - immunocytochemistry

KW - stage specific expression

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U2 - 10.1016/j.ijpara.2006.10.003

DO - 10.1016/j.ijpara.2006.10.003

M3 - Article

VL - 37

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JO - International Journal for Parasitology

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