Origin of Mitochondria and Hydrogenosomes

313 Pages·2007·4.01 MB·English

by  William F. Martin

William F. Martin Miklós Müller (Editors)
●
Origin of Mitochondria and Hydrogenosomes
William F. Martin
Miklós Müller (Editors)
Origin of Mitochondria and
Hydrogenosomes
With 31 Figures, 7 in Color and 6 Tables
Professor Dr. William F. Martin Dr. Miklós Müller
Institut für Botanik III The Rockefeller University
Heinrich-Heine Universität Düsseldorf 1230 York Avenue
Universitätsstr. 1 New York, NY 10021-6399
40225 Düsseldorf USA
Germany and
Collegium Budapest
1014 Budapest
Hungary
Cover photo:‘Hydrogenosomes 1974’ by M. Müller and H. Shio
Library of Congress Control Number: 2006933053
ISBN-10 3-540-38501-0 Springer-Verlag Berlin Heidelberg New York
ISBN-13 978-3-540-38501-1 Springer-Verlag Berlin Heidelberg New York
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Preface
At the time of their discovery over 30 years ago, it was thought that
hydrogenosomes might be a novel form of either peroxisome, endosymbioti-
cally derived organelle, or mitochondrion. For about two decades, this third
possibility had seemed the least likely of all, probably because the concept of
the mitochondrion was inextricably intertwined with the concept of oxidative
phosphorylation, an attribute altogether lacking in all manifestations of the
hydrogenosome ever found (so far). In recent years, however, it became clear
that they are, indeed, a novel form of mitochondrion.
The realization that hydrogenosomes are mitochondria does not stem
solely from experimental work specifically on hydrogenosomes. Instead, it
stems from work on eukaryotic anaerobes in general: those that have
hydrogenosomes, those that have mitosomes, and those that have anaerobi-
cally functioning mitochondria. The evolutionary significance of hydrogeno-
somes only became apparent in the context of a broader view of the molecular
commonalities shared among those organisms and their organelles. In that
sense, hydrogenosomes have helped to significantly broaden our concept of
the mitochondrion.
As far as we are aware, this is the first monograph dedicated to hydrogeno-
somes. The views presented by the authors of the present volume are their
own. We did not enter into the standard editing practice of negotiating con-
tent; all authors have had full opportunity to express their own views as they
see fit. We hope that the reader finds this volume to be worthwhile. We feel
that it is a uniquely rich source of information on eukaryotic anaerobes and
their organelles and thank all contributors heartily for their hard work in
preparing the chapters.
September, 2006
Bill Martin, Düsseldorf
Miklós Müller, Budapest
Foreword
As Miklós Müller points out in his historical introduction, the evolutionary
origins of hydrogenosomes have been the subject of considerable debate.
From early days it was apparent that hydrogenosomes had evolved on multi-
ple occasions in different eukaryotes, but from which progenitor organelle or
endosymbiont was unresolved because of sparse and sometimes ambiguous
data. Work from many different laboratories has contributed towards for-
mulating the current hypothesis that hydrogenosomes and mitosomes, their
even more reduced cousins, share common ancestry with mitochondria.
These modern discoveries can be interpreted in terms of classical evolution-
ary theory. Hydrogenosomes, mitosomes and mitochondria are evolutionary
homologues in the sense meant by Charles Darwin. Their shared similarities,
for example their common mechanisms of protein import and their double
membrane, can be explained by common ancestry, and their differences by
descent with modification under contrasting lifestyles. The hypothesis that
mitochondria, mitosomes and hydrogenosomes are homologues predicts
that, as the organelles are studied more deeply, additional shared features will
be revealed.
Understanding the origins of eukaryotic organelles and proteins is inextri-
cably linked to efforts to understand eukaryotic relationships and to the
development of more reliable phylogenetic methods. This is an area of
endeavour that demands its own expertise, since overly simple analyses can
produce strongly supported, but nevertheless incorrect, trees. Early efforts to
make phylogenetic trees using gene sequences suggested that Trichomonas, a
key model organism for understanding hydrogenosome evolution, separated
from other eukaryotes before the mitochondrial endosymbiosis. This created
a situation where it was deemed credible to suggest that the Trichomonas
hydrogenosome had an origin distinct from that of other hydrogenosomes,
through a unique endosymbiosis involving the ancestor of Trichomonasand
an anaerobic hydrogen-producing bacterium. Today, there are widely
accepted data for only two endosymbioses producing eukaryotic organelles:
the α-proteobacterial and cyanobacterial endosymbioses that gave rise to
mitochondria and primary plastids, respectively. Any evidence purporting to
support a third invasion of the eukaryotic cell producing hydrogenosomes
was thus exciting and important. But extraordinary claims need extra-
ordinary data, and recent work suggests that the phylogenetic position
viii Foreword
of Trichomonas is uncertain. By contrast, there is general agreement
thatTrichomonascontains genes derived from the mitochondrial endosym-
biont. Lastly, the key enzymes pyruvate:ferredoxin oxidoreductase and [Fe]
hydrogenase that have fuelled the separate origin hypothesis are not unique
to the Trichomonashydrogenosome. As such, they cannot logically be used to
infer a singularly independent origin for the organelle. Surprisingly, these
two proteins, in various forms and cellular compartments, have been found
in diverse other eukaryotes with, and without, hydrogenosomes. The func-
tional role/s of these proteins in organisms that do not produce hydrogen
is/are still mostly unknown, but their conservation across diverse eukaryote
genomes suggests they might be important.
The origins of eukaryotic [Fe] hydrogenase and pyruvate:ferredoxin oxi-
doreductase are part of a bigger question concerning the origins of the eubac-
terial-like genes that encode much of eukaryote metabolism. The apparent
ubiquity of mitochondrial homologues among eukaryotes suggests that the
mitochondrial endosymbiont is a prime candidate for the source of at least
some of these genes, but how many and which ones is uncertain. There are
also a number of imaginative alternative hypotheses to explain their pres-
ence: as the product of multiple lateral transfers from different prokaryotes,
or the legacy of different eubacteria that participated in eukaryogenesis.
Genomics coupled with more sophisticated phylogenetic analyses should in
principle be able to identify eukaryote gene origins, but the search is likely to
push both our data and our methods to their limits.
Which group of α-proteobacteria provided the endosymbiont is still con-
tentious, because of the aforementioned difficulties of using phylogenetics to
pinpoint ancient events. However, the apparent ubiquity of mitochondrial
homologues among eukaryotes bears testament to the importance of the
mitochondrial endosymbiosis in eukaryotic evolution. It also means that we
can no longer be sure what came first – nucleus or mitochondrion. Put
another way, prokaryote host models for the mitochondrial endosymbiosis
can no longer be so comfortably dismissed, but must be judged on their
merits as predictive hypothesis that can be tested.
Most of what is known about mitochondrial function and the importance
of mitochondria for the eukaryotic cell is drawn from the study of yeast,
mammal and plant mitochondria. Apart from oxidative phosphorylation,
other important reactions include the Krebs cycle, haem biosynthesis,
β-oxidation of fatty acids, amino acid biosynthesis and the formation and
export of iron–sulphur clusters. New roles for mitochondria in health and
disease are continually being discovered. It is already evident from biochem-
ical and genomic data that hydrogenosomes and mitosomes can have
retained only a limited subset of these reactions. It is also clear that parasites
such as Plasmodiumand Cryptosporidiumhave also greatly reduced the cod-
ing capacity and functions of organelles that are still called mitochondria.
Mitochondrial homologues exhibit a spectrum of form and function,
the breadth of which is still being uncovered because most parasites and
Foreword ix
anaerobic eukaryotes remain poorly studied. This raises important questions
concerning the fundamental importance of this compartment of endosymbi-
otic ancestry for the eukaryotic cell, its biochemical flexibility, and the limits
of organelle reduction. Comparative study of mitochondrial homologues in
all their various guises is still needed to fully resolve these questions.
However, it is already apparent from the contributions to this volume that
identifying the genetic contribution to eukaryotes of the mitochondrial
endosymbiosis and revealing the functions of its descendent organelles are
key to understanding eukaryotic biology and evolution.
Martin Embley
Newcastle, May 2006
Contents
1 The Road to Hydrogenosomes
MIKLÓSMÜLLER . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1
1.1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1
1.2 The Story . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2
1.3 Conclusion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 9
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 10
2 Mitochondria: Key to Complexity
NICKLANE . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 13
2.1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 13
2.2 Size . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 15
2.3 Compartments . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 16
2.4 Dynamics of Gene Gain and Gene Loss in Bacteria . . . . . . . . . . . . . . . 17
2.5 ATP Regulation of Bacterial Replication . . . . . . . . . . . . . . . . . . . . . . . . 21
2.6 Redox Poise Across Bioenergetic Membranes . . . . . . . . . . . . . . . . . . . . 25
2.7 Allometric Scaling of Metabolic Rate and Complexity . . . . . . . . . . . . . 29
2.8 Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 32
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 33
3 Origin, Function, and Transmission of Mitochondria
CAROLA. ALLEN, MARKVANDERGIEZEN, JOHNF. ALLEN . . . . . . . . . . . . . . . . . . 39
3.1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 39
3.2 Origins of Mitochondria . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 40
3.3 Mitochondrial Genomes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 43
3.4 The Mitochondrial Theory of Ageing . . . . . . . . . . . . . . . . . . . . . . . . . . . 45
3.5 Why Are There Genes in Mitochondria? . . . . . . . . . . . . . . . . . . . . . . . . 47
3.6 Co-location of Gene and Gene Product Permits Redox
Regulation of Gene Expression . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 48
3.7 Maternal Inheritance of Mitochondria . . . . . . . . . . . . . . . . . . . . . . . . . 50
3.8 Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 53
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 53
4 Mitochondria and Their Host: Morphology to Molecular Phylogeny
JANSAPP . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 57
4.1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 57
4.2 Alternative Visions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 57
4.3 Before the Word . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 59
xii Contents
4.4 Les Symbiotes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 60
4.5 Symbionticism and the Origin of Species . . . . . . . . . . . . . . . . . . . . . . . 62
4.6 Against the Current . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 63
4.7 Infective Heredity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 65
4.8 The Tipping Point . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 67
4.9 The Birth of Bacterial Phylogenetics . . . . . . . . . . . . . . . . . . . . . . . . . . . 69
4.10 Just-So Stories . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 70
4.11 Kingdom Come, Kingdom Go . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 71
4.12 A Chimeric Paradigm . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 74
4.13 Recapitulation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 77
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 78
5 Anaerobic Mitochondria: Properties and Origins
ALOYSIUSG.M. TIELENS, JAAPJ.VANHELLEMOND . . . . . . . . . . . . . . . . . . . . . . . . 85
5.1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 85
5.2 Possible Variants in Anaerobic Metabolism . . . . . . . . . . . . . . . . . . . . . 86
5.3 Cytosolic Adaptations to an Anaerobic Energy Metabolism . . . . . . . . 88
5.4 Anaerobically Functioning ATP-Generating Organelles . . . . . . . . . . . 89
5.5 Energy Metabolism in Anaerobically Functioning Mitochondria . . . . 90
5.6 Adaptations in Electron-Transport Chains in Anaerobic
Mitochondria . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 95
5.7 Structural Aspects of Anaerobically Functioning Electron-
Transport Chains . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 96
5.8 Evolutionary Origin of Anaerobic Mitochondria . . . . . . . . . . . . . . . . . 97
5.9 Conclusion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 100
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 100
6 Iron–Sulfur Proteins and Iron–Sulfur Cluster Assembly in Organisms
with Hydrogenosomes and Mitosomes
JANTACHEZY, PAVELDOLEZˇAL . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 105
6.1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 105
6.2 Mitochondrion-Related Organelles in “Amitochondriate”
Eukaryotes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 106
6.2.1 Hydrogenosomes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 107
6.2.2 Mitosomes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 108
6.3 Iron–Sulfur Cluster, an Ancient Indispensable Prosthetic Group . . . . 109
6.4 Iron–Sulfur Proteins in Mitochondria and Other Cell
Compartments . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 109
6.5 Iron–Sulfur Proteins in Organisms Harboring Hydrogenosomes
and Mitosomes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 110
6.6 Iron–Sulfur Cluster Assembly Machineries . . . . . . . . . . . . . . . . . . . . . . 116
6.6.1 Iron–Sulfur Cluster Assembly in Saccharomyces cerevisiae . . . 116
6.6.2 Trichomonas vaginalis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 118
6.6.3 Giardia intestinalis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 120
6.6.4 Cryptosporidium parvum . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 121
6.6.5 Microsporidia . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 122
6.6.6 Entamoeba histolytica . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 122