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How much (ATP) does it cost to build a trypanosome? A theoretical study on the quantity of ATP needed to maintain and duplicate a bloodstream-form Trypanosoma brucei cell

ATP hydrolysis is required for the synthesis, transport and polymerization of monomers for macromolecules as well as for the assembly of the latter into cellular structures. Other cellular processes not directly related to synthesis of biomass, such as maintenance of membrane potential and cellular...

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Autores principales: Nascimento, Janaina F., Souza, Rodolpho O. O., Alencar, Mayke B., Marsiccobetre, Sabrina, Murillo, Ana M., Damasceno, Flávia S., Girard, Richard B. M. M., Marchese, Letícia, Luévano-Martinez, Luis A., Achjian, Renan W., Haanstra, Jurgen R., Michels, Paul A. M., Silber, Ariel M.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10409291/
https://www.ncbi.nlm.nih.gov/pubmed/37498954
http://dx.doi.org/10.1371/journal.ppat.1011522
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author Nascimento, Janaina F.
Souza, Rodolpho O. O.
Alencar, Mayke B.
Marsiccobetre, Sabrina
Murillo, Ana M.
Damasceno, Flávia S.
Girard, Richard B. M. M.
Marchese, Letícia
Luévano-Martinez, Luis A.
Achjian, Renan W.
Haanstra, Jurgen R.
Michels, Paul A. M.
Silber, Ariel M.
author_facet Nascimento, Janaina F.
Souza, Rodolpho O. O.
Alencar, Mayke B.
Marsiccobetre, Sabrina
Murillo, Ana M.
Damasceno, Flávia S.
Girard, Richard B. M. M.
Marchese, Letícia
Luévano-Martinez, Luis A.
Achjian, Renan W.
Haanstra, Jurgen R.
Michels, Paul A. M.
Silber, Ariel M.
author_sort Nascimento, Janaina F.
collection PubMed
description ATP hydrolysis is required for the synthesis, transport and polymerization of monomers for macromolecules as well as for the assembly of the latter into cellular structures. Other cellular processes not directly related to synthesis of biomass, such as maintenance of membrane potential and cellular shape, also require ATP. The unicellular flagellated parasite Trypanosoma brucei has a complex digenetic life cycle. The primary energy source for this parasite in its bloodstream form (BSF) is glucose, which is abundant in the host’s bloodstream. Here, we made a detailed estimation of the energy budget during the BSF cell cycle. As glycolysis is the source of most produced ATP, we calculated that a single parasite produces 6.0 x 10(11) molecules of ATP/cell cycle. Total biomass production (which involves biomass maintenance and duplication) accounts for ~63% of the total energy budget, while the total biomass duplication accounts for the remaining ~37% of the ATP consumption, with in both cases translation being the most expensive process. These values allowed us to estimate a theoretical Y(ATP) of 10.1 (g biomass)/mole ATP and a theoretical [Image: see text] of 28.6 (g biomass)/mole ATP. Flagellar motility, variant surface glycoprotein recycling, transport and maintenance of transmembrane potential account for less than 30% of the consumed ATP. Finally, there is still ~5.5% available in the budget that is being used for other cellular processes of as yet unknown cost. These data put a new perspective on the assumptions about the relative energetic weight of the processes a BSF trypanosome undergoes during its cell cycle.
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spelling pubmed-104092912023-08-09 How much (ATP) does it cost to build a trypanosome? A theoretical study on the quantity of ATP needed to maintain and duplicate a bloodstream-form Trypanosoma brucei cell Nascimento, Janaina F. Souza, Rodolpho O. O. Alencar, Mayke B. Marsiccobetre, Sabrina Murillo, Ana M. Damasceno, Flávia S. Girard, Richard B. M. M. Marchese, Letícia Luévano-Martinez, Luis A. Achjian, Renan W. Haanstra, Jurgen R. Michels, Paul A. M. Silber, Ariel M. PLoS Pathog Research Article ATP hydrolysis is required for the synthesis, transport and polymerization of monomers for macromolecules as well as for the assembly of the latter into cellular structures. Other cellular processes not directly related to synthesis of biomass, such as maintenance of membrane potential and cellular shape, also require ATP. The unicellular flagellated parasite Trypanosoma brucei has a complex digenetic life cycle. The primary energy source for this parasite in its bloodstream form (BSF) is glucose, which is abundant in the host’s bloodstream. Here, we made a detailed estimation of the energy budget during the BSF cell cycle. As glycolysis is the source of most produced ATP, we calculated that a single parasite produces 6.0 x 10(11) molecules of ATP/cell cycle. Total biomass production (which involves biomass maintenance and duplication) accounts for ~63% of the total energy budget, while the total biomass duplication accounts for the remaining ~37% of the ATP consumption, with in both cases translation being the most expensive process. These values allowed us to estimate a theoretical Y(ATP) of 10.1 (g biomass)/mole ATP and a theoretical [Image: see text] of 28.6 (g biomass)/mole ATP. Flagellar motility, variant surface glycoprotein recycling, transport and maintenance of transmembrane potential account for less than 30% of the consumed ATP. Finally, there is still ~5.5% available in the budget that is being used for other cellular processes of as yet unknown cost. These data put a new perspective on the assumptions about the relative energetic weight of the processes a BSF trypanosome undergoes during its cell cycle. Public Library of Science 2023-07-27 /pmc/articles/PMC10409291/ /pubmed/37498954 http://dx.doi.org/10.1371/journal.ppat.1011522 Text en © 2023 Nascimento et al https://creativecommons.org/licenses/by/4.0/This is an open access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Nascimento, Janaina F.
Souza, Rodolpho O. O.
Alencar, Mayke B.
Marsiccobetre, Sabrina
Murillo, Ana M.
Damasceno, Flávia S.
Girard, Richard B. M. M.
Marchese, Letícia
Luévano-Martinez, Luis A.
Achjian, Renan W.
Haanstra, Jurgen R.
Michels, Paul A. M.
Silber, Ariel M.
How much (ATP) does it cost to build a trypanosome? A theoretical study on the quantity of ATP needed to maintain and duplicate a bloodstream-form Trypanosoma brucei cell
title How much (ATP) does it cost to build a trypanosome? A theoretical study on the quantity of ATP needed to maintain and duplicate a bloodstream-form Trypanosoma brucei cell
title_full How much (ATP) does it cost to build a trypanosome? A theoretical study on the quantity of ATP needed to maintain and duplicate a bloodstream-form Trypanosoma brucei cell
title_fullStr How much (ATP) does it cost to build a trypanosome? A theoretical study on the quantity of ATP needed to maintain and duplicate a bloodstream-form Trypanosoma brucei cell
title_full_unstemmed How much (ATP) does it cost to build a trypanosome? A theoretical study on the quantity of ATP needed to maintain and duplicate a bloodstream-form Trypanosoma brucei cell
title_short How much (ATP) does it cost to build a trypanosome? A theoretical study on the quantity of ATP needed to maintain and duplicate a bloodstream-form Trypanosoma brucei cell
title_sort how much (atp) does it cost to build a trypanosome? a theoretical study on the quantity of atp needed to maintain and duplicate a bloodstream-form trypanosoma brucei cell
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10409291/
https://www.ncbi.nlm.nih.gov/pubmed/37498954
http://dx.doi.org/10.1371/journal.ppat.1011522
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