Rewiring and regulation of cross-compartmentalized metabolism in protists

Michael L. Ginger, Geoffrey I. McFadden, Paul A.M. Michels

Research output: Contribution to journalReview article

37 Citations (Scopus)

Abstract

Plastid acquisition, endosymbiotic associations, lateral gene transfer, organelle degeneracy or even organelle loss influence metabolic capabilities in many different protists. Thus, metabolic diversity is sculpted through the gain of new metabolic functions and moderation or loss of pathways that are often essential in the majority of eukaryotes. What is perhaps less apparent to the casual observer is that the sub-compartmentalization of ubiquitous pathways has been repeatedly remodelled during eukaryotic evolution, and the textbook pictures of intermediary metabolism established for animals, yeast and plants are not conserved in many protists. Moreover, metabolic remodelling can strongly influence the regulatory mechanisms that control carbon flux through the major metabolic pathways. Here, we provide an overview of how core metabolism has been reorganized in various unicellular eukaryotes, focusing in particular on one near universal catabolic pathway (glycolysis) and one ancient anabolic pathway (isoprenoid biosynthesis). For the example of isoprenoid biosynthesis, the compartmentalization of this process in protists often appears to have been influenced by plastid acquisition and loss, whereas for glycolysis several unexpected modes of compartmentalization have emerged. Significantly, the example of trypanosomatid glycolysis illustrates nicely how mathematical modelling and systems biology can be used to uncover or understand novel modes of pathway regulation.

LanguageEnglish
Pages831-845
Number of pages15
JournalPhilosophical Transactions of the Royal Society B: Biological Sciences
Volume365
Issue number1541
Early online date2 Feb 2010
DOIs
Publication statusPublished - 12 Mar 2010
Externally publishedYes

Fingerprint

glycolysis
Glycolysis
Metabolism
Plastids
isoprenoids
Biosynthesis
Terpenes
Eukaryota
Organelles
plastids
metabolism
organelles
eukaryotic cells
biosynthesis
Gene transfer
Trypanosomatidae
Carbon Cycle
Horizontal Gene Transfer
Systems Biology
Textbooks

Cite this

@article{7d6c8416dafc4a4091adcf60354320df,
title = "Rewiring and regulation of cross-compartmentalized metabolism in protists",
abstract = "Plastid acquisition, endosymbiotic associations, lateral gene transfer, organelle degeneracy or even organelle loss influence metabolic capabilities in many different protists. Thus, metabolic diversity is sculpted through the gain of new metabolic functions and moderation or loss of pathways that are often essential in the majority of eukaryotes. What is perhaps less apparent to the casual observer is that the sub-compartmentalization of ubiquitous pathways has been repeatedly remodelled during eukaryotic evolution, and the textbook pictures of intermediary metabolism established for animals, yeast and plants are not conserved in many protists. Moreover, metabolic remodelling can strongly influence the regulatory mechanisms that control carbon flux through the major metabolic pathways. Here, we provide an overview of how core metabolism has been reorganized in various unicellular eukaryotes, focusing in particular on one near universal catabolic pathway (glycolysis) and one ancient anabolic pathway (isoprenoid biosynthesis). For the example of isoprenoid biosynthesis, the compartmentalization of this process in protists often appears to have been influenced by plastid acquisition and loss, whereas for glycolysis several unexpected modes of compartmentalization have emerged. Significantly, the example of trypanosomatid glycolysis illustrates nicely how mathematical modelling and systems biology can be used to uncover or understand novel modes of pathway regulation.",
keywords = "Glycolysis, Glycosomes, Isoprenoid biosynthesis, Mitochondria, Organelle evolution, Plastids",
author = "Ginger, {Michael L.} and McFadden, {Geoffrey I.} and Michels, {Paul A.M.}",
year = "2010",
month = "3",
day = "12",
doi = "10.1098/rstb.2009.0259",
language = "English",
volume = "365",
pages = "831--845",
journal = "Philosophical Transactions of the Royal Society B: Biological Sciences",
issn = "0800-4622",
publisher = "Royal Society of London",
number = "1541",

}

Rewiring and regulation of cross-compartmentalized metabolism in protists. / Ginger, Michael L.; McFadden, Geoffrey I.; Michels, Paul A.M.

In: Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 365, No. 1541, 12.03.2010, p. 831-845.

Research output: Contribution to journalReview article

TY - JOUR

T1 - Rewiring and regulation of cross-compartmentalized metabolism in protists

AU - Ginger, Michael L.

AU - McFadden, Geoffrey I.

AU - Michels, Paul A.M.

PY - 2010/3/12

Y1 - 2010/3/12

N2 - Plastid acquisition, endosymbiotic associations, lateral gene transfer, organelle degeneracy or even organelle loss influence metabolic capabilities in many different protists. Thus, metabolic diversity is sculpted through the gain of new metabolic functions and moderation or loss of pathways that are often essential in the majority of eukaryotes. What is perhaps less apparent to the casual observer is that the sub-compartmentalization of ubiquitous pathways has been repeatedly remodelled during eukaryotic evolution, and the textbook pictures of intermediary metabolism established for animals, yeast and plants are not conserved in many protists. Moreover, metabolic remodelling can strongly influence the regulatory mechanisms that control carbon flux through the major metabolic pathways. Here, we provide an overview of how core metabolism has been reorganized in various unicellular eukaryotes, focusing in particular on one near universal catabolic pathway (glycolysis) and one ancient anabolic pathway (isoprenoid biosynthesis). For the example of isoprenoid biosynthesis, the compartmentalization of this process in protists often appears to have been influenced by plastid acquisition and loss, whereas for glycolysis several unexpected modes of compartmentalization have emerged. Significantly, the example of trypanosomatid glycolysis illustrates nicely how mathematical modelling and systems biology can be used to uncover or understand novel modes of pathway regulation.

AB - Plastid acquisition, endosymbiotic associations, lateral gene transfer, organelle degeneracy or even organelle loss influence metabolic capabilities in many different protists. Thus, metabolic diversity is sculpted through the gain of new metabolic functions and moderation or loss of pathways that are often essential in the majority of eukaryotes. What is perhaps less apparent to the casual observer is that the sub-compartmentalization of ubiquitous pathways has been repeatedly remodelled during eukaryotic evolution, and the textbook pictures of intermediary metabolism established for animals, yeast and plants are not conserved in many protists. Moreover, metabolic remodelling can strongly influence the regulatory mechanisms that control carbon flux through the major metabolic pathways. Here, we provide an overview of how core metabolism has been reorganized in various unicellular eukaryotes, focusing in particular on one near universal catabolic pathway (glycolysis) and one ancient anabolic pathway (isoprenoid biosynthesis). For the example of isoprenoid biosynthesis, the compartmentalization of this process in protists often appears to have been influenced by plastid acquisition and loss, whereas for glycolysis several unexpected modes of compartmentalization have emerged. Significantly, the example of trypanosomatid glycolysis illustrates nicely how mathematical modelling and systems biology can be used to uncover or understand novel modes of pathway regulation.

KW - Glycolysis

KW - Glycosomes

KW - Isoprenoid biosynthesis

KW - Mitochondria

KW - Organelle evolution

KW - Plastids

UR - http://www.scopus.com/inward/record.url?scp=77349121030&partnerID=8YFLogxK

U2 - 10.1098/rstb.2009.0259

DO - 10.1098/rstb.2009.0259

M3 - Review article

VL - 365

SP - 831

EP - 845

JO - Philosophical Transactions of the Royal Society B: Biological Sciences

T2 - Philosophical Transactions of the Royal Society B: Biological Sciences

JF - Philosophical Transactions of the Royal Society B: Biological Sciences

SN - 0800-4622

IS - 1541

ER -