Hydrogenosomes and Mitosomes: Mitochondria of Anaerobic Eukaryotes

295 Pages·2008·5.26 MB·English

by  William Martin (auth.)

9
Microbiology Monographs
SeriesEditor:Alexander Steinbüchel
MicrobiologyMonographs
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Hydrogenosomes and Mitosomes:
Mitochondria of Anaerobic Eukaryotes
Volume Editor: Jan Tachezy
123
VolumeEditor:
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ISBN978-3-540-76732-9 e-ISBN978-3-540-76733-6
DOI10.1007/978-3-540-76733-6
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Preface
Hydrogenosomes represent a group of double membrane-bound organelles
that have the production of molecular hydrogen and ATP in common. Such
awelldefinedfeatureisunknownforanothertypeofdoublemembrane-bound
organellescalledbyvariousnamessuchasmitosomes,cryptons,remnantmi-
tochondriaormitochondria-likeorganelles.Theseorganellesneitherproduce
hydrogennorsynthetizeATPandweknowlittleabouttheirfunctions,except
the biogenesis of iron-sulfur clusters found in some of them. The common
denominator for both hydrogenosomesand mitosomesis their evolutionary
origin. It is generally accepted that both hydrogenosomes and mitosomes
evolvedfrommitochondriaoranancestralpre-mitochondrialendosymbiont
(discussedbyBillMartininthisvolume).Withourgrowingknowledgeabout
hydrogenosomes and mitosomes it is also becoming apparent that it will be
difficulttodrawaclearlydefinedlinebetweenmitochondria,hydrogenosomes
andmitosomes.Aswebelieveandasthetitleofthisvolumeindicates,allthese
organellesareakindofmitochondriainabroadsense,andthereasonfortheir
differentnamesisprimarilyhistorical.Inlinewiththishypothesis,thename
“amitochondriates” should no longer be used for the organisms possessing
hydrogenosomesandmitosomes,sincethistermreferstoanallegedabsence
ofmitochondria.
Wewouldliketothankalltheauthorswhocontributedoutstandingchap-
tersabouthydrogenosomesandmitosomestothisMicrobiologyMonographs
volume summarizing current knowledge about evolution, biogenesis, struc-
tureandfunctionoftheseexciting organelles.Wehighlyappreciate thetime
and effort that the authors invested in the preparation of their manuscripts.
Althoughthisformofpublicationisusuallynotscoredbygrantagencies,itis
essentialinprovidingcomprehensiveinformationtoreadersworkinginother
fieldsofbiologyandinattractingyoungscientistsandstudentsinterestedin
thefieldofprotistcellbiology.
WewouldliketodedicatethisvolumetoMiklósMüllerandJaroslavKulda
whotogetherwiththeircolleagues(DonaldLindmark,ApolenaCˇerkasovová,
Jiˇrí Cˇerkasov) offered the first description of hydrogenosomes in the early
1970s.Althoughvariousnewhydrogenosomalpathwaysandcomponentshave
sincebeenrevealed(especiallybyrecentgenomicandproteomicstudies),the
VI Preface
basicmetabolicpathwaysuncoveredinpioneeringbiochemicalstudiesintheir
laboratoriesinNewYorkandPragueremain abackboneofhydrogenosomal
metabolismintrichomonads.
PragueandMünster,December2007 JanTachezy
AlexanderSteinbüchel
Introduction
,,Esistschlimmgenug,”riefEduard,
,,dassmanjetztnichtmehrfürseinganzesLebenlernenkann.
UnsereVorfahrenhieltensichandenUnterricht,
densieinihrereJugendempfangen;
wirabermüssenjetztallefünfJahreumlernen,
wennwirnichtganzausderModekommenwollen.”
JohannWolfgangGoethe,DieWahlverwandschaften,1807
“Itisbadenough,”saidEduard,
“thatourlearningdoesnotlastforourwholelife.
Ourancestorscouldholdontothelearningthattheyacquiredintheiryouth;
wehavetorelearneverythingeveryfiveyears,justtoremainfashionable.”
(Author’stranslation)
Thisvolumesummarizesourknowledgeonagroupofdiverseand“unusual”
cellorganelles. Itispublished atamostappropriatetime when itseems that
a consensus is emerging about the nature of these entities. Evidence accu-
mulating over the past few years has brought home the prodigal sons of the
mitochondrial family. Hydrogenosomes and mitosomes are now within the
foldofthewell-knownandrespectedorganellefamilythatincludesthe“pow-
erhouses”oftheaerobiceukaryoticworld.Chapters inthisbookdescribein
detail these organelles which exhibit a bewildering array of characteristics
butaccordingtoanemerging consensusofmostbiologistsallaremitochon-
driaindifferentguises.Theyareassumedtorepresentamonophyleticgroup
of biological entities that originated from an ancestral endosymbiotic event
thatgave risetotheprotomitochondrion.Ofcoursetheemerging consensus
does not mean that there are no dissenters in many quarters of the biology
community. What convincingarguments today might not turnout tobe red
herringstomorrow?Thehistoryofthepast30orsoyearsgivesamplewarning.
Ourviewsandtheoriesrelatedtothisfieldhavechangeddrasticallysomany
VIII Introduction
timesduringtheseyearsthatwecannotbecertainthatfuturesurprisesarenot
lurkingaroundthecorner.
Atanyrate,thisbooktakesstockofthestatusquo.Itpresentsacastconsist-
ingofdouble-membraneboundedorganellesofeukaryoticprotistsandfungi,
whichliveunderanaerobicorhypoxicconditions,aswellascertainintracel-
lularparasitesofaerobiccells.Thecommondenominatoroftheseorganelles
isthattheylacktheaerobicenergyconservationsystemoftypicalmitochon-
dria, i.e. the cytochrome-dependent electron transport chain and oxidative
phosphorylation.Anothercommondenominatoristhat—onecuriousexcep-
tiondisregarded—they arethe site of a process, thesynthesis ofiron–sulfur
clusters, whichisregardedtodayastheonlyreallyindispensable functionof
eukaryotic mitochondria. These organelles exhibit, however, properties and
characteristics in so many different combinations that all generalizations of
thegroup(beyondthejust-mentionedmajornegativeandpositivehallmarks)
wouldbefutile, i.e. any general definitionwouldrequire morequalifications
thanunequivocalstatements.
As evident fromthe individual chapters, the major members of this fam-
ily are the mitosomes, small organelles without a known role in energy
metabolism, and the hydrogenosomes, organelles of the approximate size of
mitochondria, characterized by their ability to produce molecular hydrogen
as a metabolic end product. Recent evidence, however, has revealed that the
latter organelles can be quite different, anywhere fromtypical mitochondria
toorganellesthatdonotresemblemitochondriaatall.Theindividual differ-
enceswithinthesegroupsaresogreat,andtheboundariesbetween themso
undefined, thatnogenerallyacceptablenomenclaturehasyetemerged. Each
investigatorusesadifferentdesignationforhis/herorganelle.
I wish to emphasize the perhaps most significant aspect of the emerging
consensus. The distribution of these organelles in the living world is broad.
They arefoundincertainmembers ofalmostallofthecurrently recognized
majorevolutionarylineagesofeukaryotes.Theirpresenceseemstobeprimar-
ilycorrelatedwiththeecologyoftheorganisms,whichliveinananoxichabitat
orinanutrient-richintracellularnichethatpermitslifewithouttheefficient
energy-generating system of typical mitochondria. This distribution argues
stronglyforthehypothesisthatdiversemitosomesandhydrogenosomesarose
independently, and repeatedly, during the diversification of the eukaryotes.
Convergentevolutioninaction!Italsoarguesstronglyagainst theearlieras-
sumption that the presence of these organelles could represent an ancestral,
pre-mitochondrialstate.
Asmentionedabove,theroadleadinguptothepresentstateofaffairswas
convoluted, andoftenterminated in dead-end streets. Wehadtochangeour
views and hypotheses repeatedly, had to relearn everything, just as Eduard
wasrequiredtorelearneverythingtwocenturiesago.Thisforewordisnotthe
placetorecountthehistoryofourviewsoftheseorganelles.Igaveanaccount
oftheeventsleadinguptothefirstdescriptionofahydrogenosomeinanother
Introduction IX
place(Müller,2007),andsoIhopethatsomeonewilltellusthestoryasithas
unfoldedduringtheinterveningyears.
I wish to add some personal remarks here. I was very pleased when the
editorofthisvolume,HonzaTachezy,askedmetowriteabriefforewordand
Ithank him very much. Iam certain that thisbookwillplay amajor rolein
thefuturedevelopment ofthisexcitingareaofcomparativeandevolutionary
biology.LittledidDonLindmarkandIthinkin1973thatourdescriptionofan
unusualcellorganellefromagroupofoddparasiteswouldgivethefirstpush
totheunfoldingofwhatturnedouttobeamostexcitingstoryinevolutionary
cellbiology(LindmarkandMüller,1973).Itisagreatpersonalsatisfactionto
me,andIamsure,toallthosewhowerewithmeatvarioustimes,toseewhere
ourendeavorshaveled.Ilookforwardtoseeingwhatthefutureholds.
Lastly, I wish to acknowledge the unfailing support and friendship of my
mentorChristiandeDuve.ItwasinhisDepartmentatRockefellerUniversity
where Donand I performed the initial experiments, and where I have spent
manyproductiveyears.Iwouldliketothankallthepastmembersofmygroup
whowereresponsibleforalltheirownworkontheseorganelles.Ialsothank
allthosecolleaguesworkingindiversepartsoftheworldwhobelievedinthe
promise this field held and carried the torchfurther. I received much moral
supportfromthem,however,theyaretoonumeroustobenamedhere.Ialso
acknowledgetheuninterruptedsupportofouroriginalworkattheRockefeller
Universityforalmost30yearsbythesameNIHgrant(AI11942) andalsoby
severalgrantsfromNSF.
TheRockefellerUniversity,NewYork
andCollegiumBudapest,Budapest,September2007 MiklósMüller
References
LindmarkDG,MüllerM(1973) Hydrogenosome, acytoplasmicorganelleoftheanaero-
bicflagellate,Tritrichomonasfoetus,anditsroleinpyruvatemetabolism.JBiolChem
248:7724–7728
MüllerM(2007)Theroadtohydrogenosomes. In:MartinWF,MüllerM(eds)Originof
mitochondriaandhydrogenosomes.Springer,BerlinHeidelbergNewYork,pp1–11