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

doi:10.1016/j.ijpara.2006.10.003

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

Bloomberg School of Public Health

Research output: Contribution to journal › Article › peer-review

36 Scopus citations

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.

Original language	English (US)
Pages (from-to)	33-51
Number of pages	19
Journal	International Journal for Parasitology
Volume	37
Issue number	1
DOIs	https://doi.org/10.1016/j.ijpara.2006.10.003
State	Published - Jan 2007

Keywords

Apicoplast
Eimeria tenella
Enoyl reductase
Immunocytochemistry
Stage specific expression

ASJC Scopus subject areas

Parasitology
Infectious Diseases

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10.1016/j.ijpara.2006.10.003

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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. (2007). Enzymes of type II fatty acid synthesis and apicoplast differentiation and division in Eimeria tenella. International Journal for Parasitology, 37(1), 33-51. https://doi.org/10.1016/j.ijpara.2006.10.003

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

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title = "Enzymes of type II fatty acid synthesis and apicoplast differentiation and division in Eimeria tenella",

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.",

keywords = "Apicoplast, Eimeria tenella, Enoyl reductase, Immunocytochemistry, Stage specific expression",

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

note = "Funding Information: This work was supported by NIH grants R01 AI43228 (R.M. and C.W.R.) and AI27530 (R.M.), the Research to Prevent Blindness Foundation (R.M.) and a Wellcome Trust equipment grant (D.J.P.F). Ms. H. Beard is thanked for assistance in preparing the diagram in Fig. 9 . ",

year = "2007",

month = jan,

doi = "10.1016/j.ijpara.2006.10.003",

language = "English (US)",

volume = "37",

pages = "33--51",

journal = "International Journal for Parasitology",

issn = "0020-7519",

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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.

N1 - Funding Information: This work was supported by NIH grants R01 AI43228 (R.M. and C.W.R.) and AI27530 (R.M.), the Research to Prevent Blindness Foundation (R.M.) and a Wellcome Trust equipment grant (D.J.P.F). Ms. H. Beard is thanked for assistance in preparing the diagram in Fig. 9 .

PY - 2007/1

Y1 - 2007/1

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 - Apicoplast

KW - Eimeria tenella

KW - Enoyl reductase

KW - Immunocytochemistry

KW - Stage specific expression

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

Abstract

Keywords

ASJC Scopus subject areas

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