Lipid Biology of Archaea - Hindawi Publishing Corporation

92 Pages·2012·7.77 MB·English

Archaea
Lipid Biology of Archaea
Guest Editors: Angela Corcelli, Parkson Lee-Gau Chong,
and Yosuke Koga
Lipid Biology of Archaea
Archaea
Lipid Biology of Archaea
Guest Editors: Angela Corcelli, Parkson Lee-Gau Chong,
and Yosuke Koga
Copyright©2012HindawiPublishingCorporation.Allrightsreserved.
Thisisaspecialissuepublishedin“Archaea.”AllarticlesareopenaccessarticlesdistributedundertheCreativeCommonsAttribution
License,whichpermitsunrestricteduse,distribution,andreproductioninanymedium,providedtheoriginalworkisproperlycited.
Editorial Board
MaqsudulAlam,USA DennisW.Grogan,USA AllaNozhevnikova,Russia
Sonja-VerenaAlbers,Germany RobertP.Gunsalus,USA FrancescaM.Pisani,Italy
RicardoAmils,Spain ReinhardHensel,Germany MarinaPorcelli,Italy
HaruyukiAtomi,Japan LiHuang,China DavidPrangishvili,France
N.K.Birkeland,Norway MichaelIbba,USA ReinhardRachel,Germany
PaulH.Blum,USA YoshizumiIshino,Japan Anna-LouiseReysenbach,USA
E.Bonch-Osmolovskaya,Russia ToshioIwasaki,Japan FrankT.Robb,USA
Mar´ıaJose´ Bonete,Spain ZviKelman,USA F.Rodriguez-Valera,Spain
GiovannaCacciapuoti,Italy Serve´ Kengen,TheNetherlands RobertoScandurra,Italy
IsaacK.O.Cann,USA Hans-PeterKlenk,Germany KevinR.Sowers,USA
Danie¨lCharlier,Belgium PaolaLondei,Italy StefanSpring,Germany
AntoineDanchin,France PeterA.Lund,UK MichaelThomm,Germany
UweDeppenmeier,Germany GiuseppeManco,Italy HermanvanTilbeurgh,France
NejatDu¨zgu¨nes,USA WilliamW.Metcalf,USA A.Ventosa,Spain
JerryEichler,Israel MarcoMoracci,Italy WilliamB.Whitman,USA
HaraldEngelhardt,Germany MasaakiMorikawa,Japan MasafumiYohda,Japan
MichaelW.Friedrich,Germany VolkerMueller,Germany ChuanlunZhang,USA
ToshiakiFukui,Japan BiswarupMukhopadhyay,USA C.Zwieb,USA
RogerGarrett,Denmark KatsuhikoMurakami,USA
Contents
LipidBiologyofArchaea,AngelaCorcelli,ParksonLee-GauChong,andYosukeKoga
Volume2012,ArticleID710836,2pages
PhylogenomicInvestigationofPhospholipidSynthesisinArchaea,JonathanLombard,
Purificacio´nLo´pez-Garc´ıa,andDavidMoreira
Volume2012,ArticleID630910,13pages
CoupledTLCandMALDI-TOF/MSAnalysesoftheLipidExtractoftheHyperthermophilicArchaeon
Pyrococcusfuriosus,SimonaLobasso,PatriziaLopalco,RobertoAngelini,RitaVitale,HaraldHuber,
VolkerMu¨ller,andAngelaCorcelli
Volume2012,ArticleID957852,10pages
SyntheticArchaeosomeVaccinesContainingTriglycosylarchaeolsCanProvideAdditiveand
Long-LastingImmuneResponsesThatAreEnhancedbyArchaetidylserine,G.DennisSprott,
AngelaYeung,ChantalJ.Dicaire,SiuH.Yu,andDennisM.Whitfield
Volume2012,ArticleID513231,9pages
LipidsofArchaealViruses,ElinaRoineandDennisH.Bamford
Volume2012,ArticleID384919,8pages
OnPhysicalPropertiesofTetraetherLipidMembranes:EffectsofCyclopentaneRings,
ParksonLee-GauChong,UmmeAyesa,VarshaPrakashDaswani,andEllahChayHur
Volume2012,ArticleID138439,11pages
ThermalAdaptationoftheArchaealandBacterialLipidMembranes,YosukeKoga
Volume2012,ArticleID789652,6pages
EffectofGrowthMediumpHofAeropyrumpernixonStructuralPropertiesandFluidityof
Archaeosomes,AjdaOta,DejanGmajner,MarjetaSˇentjurc,andNatasˇaPoklarUlrih
Volume2012,ArticleID285152,9pages
NovelCardiolipinsfromUnculturedMethane-MetabolizingArchaea,MarcosY.Yoshinaga,LarsWo¨rmer,
MarcusElvert,andKai-UweHinrichs
Volume2012,ArticleID832097,9pages
ArchaealPhospholipidBiosyntheticPathwayReconstructedinEscherichiacoli,TakeruYokoi,
KeisukeIsobe,TohruYoshimura,andHisashiHemmi
Volume2012,ArticleID438931,9pages
HindawiPublishingCorporation
Archaea
Volume2012,ArticleID710836,2pages
doi:10.1155/2012/710836
Editorial
Lipid Biology of Archaea
AngelaCorcelli,1ParksonLee-GauChong,2andYosukeKoga3
1DepartmentofBasicMedicalSciences,UniversityofBariAldoMoro,PiazzaG.Cesare,70124Bari,Italy
2DepartmentofBiochemistry,TempleUniversitySchoolofMedicine,3420NorthBroadStreet,Philadelphia,PA19140,USA
3DepartmentofChemistry,UniversityofOccupationalandEnvironmentalHealth,Yahatanishi-ku,Kitakyushu807-8555,Japan
CorrespondenceshouldbeaddressedtoAngelaCorcelli,[email protected]
Received13November2012;Accepted13November2012
Copyright©2012Angela Corcelli et al. This is an open access article distributed under the Creative Commons Attribution
License,whichpermitsunrestricteduse,distribution,andreproductioninanymedium,providedtheoriginalworkisproperly
cited.
Today,thereisincreasingawarenessofthemultipledynamic chemical properties and biotechnological applications of
rolesoflipidsincelllife. archaeal lipids, mass spectrometry lipid analyses and lipids
Knowing how lipid molecular species are organized, ofthearchaealviruses.
interactwithproteins,andchangewithenvironmentalstress An updated phylogenic analysis of enzymes involved in
and metabolic state is crucial to understanding the mem- archaealphospholipidbiosyntheticpathwaysispresentedby
branestructureandthecellularfunctions. the group of D. Moreira. The biosynthetic pathways have
The present view of lipid biology arises from the avail- also been analyzed from the experimental point of view in
abilityoftechnologiesabletodetectevenminorlipidcom- a study of the group of H. Hemmii, which has expressed 4
ponentswithshortlifetimes.Inthelate1990s,thetechnical genesinvolvedinthebiosynthesisofarchaealphospholipids
innovation in mass spectrometry led to the development inE.coliresultingintheproductionofarchaeal-typelipidsin
of “lipidomics” as an evolution of lipid biochemistry. Fur- thebacterium;inthefuturesuchengineeredE.colicellsmay
thermore, progress in microscopy and the availability of servetotestthepropertiesofmixedmembranesconstituted
many types of fluorescent probes, together with genetic ofbotharchaealandbacterialphospholipids.
engineering, presently offer the possibility to move quickly Lipid components of the membranes of Pyrococcus
towards lipid systems biology. As a consequence, besides furiosus have been analyzed by MALDI/TOF-MS coupled
beingabletoanalyzemajorandminorlipidsofallstructures to TLC in a study of S. Lobasso et al.; while lipids of
and sizes by mass spectrometry and nuclear magnetic unculturedmethanogenspresentingeologicalsampleshave
resonance, we can study topology, structural organization, been detailed characterized by ESI-MS by M. Y. Yoshinaga
anddynamicsoflipidsbymicroscopyandfluorescentprobes etal.
inlivingcellsandmicrobes. Theabilityofarchaeallipidstoactasadjuvantinvaccines
Lipids are among the taxonomic traits that can be used designed to give protection against solid tumor has been
to clearly delineate the archaea from all other organisms. examinedinastudybyG.D.Sprottetal.
Archaealphospholipidsarebuiltonglycero-1-phosphateand AreviewarticlebyE.RoineandD.H.Bamforddescribes
contain ether-linked isoprenoid chains, while bacterial and thespecificlipidcomponentsofviralmembranesofarchaeal
eukaryal lipids are constituted of fatty acids ester-linked viruses,intheframeoftheirpossiblefunctionalrolesinthe
to glycero-3-phosphate. The radical structural differences mechanismofinfection.
between lipids of archaea and bacteria or eukaryotes raise The chemical physical properties of the lipid core of
manyquestionsaboutearlyevolutionofcellmembranes. membranesconstitutedofarchaealdietherlipidshavebeen
This special issue contains selected papers dealing examined in a study by A. Ota et al. by using fluorescence
with archaeal phospholipid biosynthetic pathways, physical steady-stateanisotropyandelectronparamagneticresonance
2 Archaea
measurements and in a review article of P. L. Chong et al.
where the role of cyclopentane rings in the lipid chains of
tetraetherlipidsonmembranefluidityisexamined.
Finally an interesting contribution of Y. Koga compar-
atively examines the different mode of adaptation to high
temperature of archaea and bacteria pointing out the role
that differences in chemical physical properties of archaeal
andbacteriallipidsmighthaveplayedinthedifferentiation
ofarchaeaandbacteriaduringevolution.
Wehopethatthisissuewillcontributetotheunderstand-
ingofthemultiplerolesoflipidsinthecellbiologyofarchaea
andwillstimulatefurtherinvestigationinthisfield,opened
bythepioneeringstudiesofMorrisKatesinthe60s.
AngelaCorcelli
ParksonLee-GauChong
YosukeKoga
HindawiPublishingCorporation
Archaea
Volume2012,ArticleID630910,13pages
doi:10.1155/2012/630910
Review Article
Phylogenomic Investigation of Phospholipid Synthesis in Archaea
JonathanLombard,Purificacio´nLo´pez-Garcı´a,andDavidMoreira
Unit´ed’EcologieSyst´ematiqueetEvolution,CNRSUMR8079,Universit´eParis-Sud,91405OrsayCedex,France
CorrespondenceshouldbeaddressedtoDavidMoreira,[email protected]
Received8August2012;Accepted3September2012
AcademicEditor:AngelaCorcelli
Copyright©2012JonathanLombardetal. This is an open access article distributed under the Creative Commons Attribution
License,whichpermitsunrestricteduse,distribution,andreproductioninanymedium,providedtheoriginalworkisproperly
cited.
Archaeahaveidiosyncraticcellmembranesusuallybasedonphospholipidscontainingglycerol-1-phosphatelinkedbyetherbonds
to isoprenoid lateral chains. Since these phospholipids strongly differ from those of bacteria and eukaryotes, the origin of the
archaealmembranes(andbyextension,ofallcellularmembranes)wasenigmaticandcalledforaccurateevolutionarystudies.
Inthispaperwereviewsomerecentphylogenomicstudiesthathaverevealedamodifiedmevalonatepathwayforthesynthesis
ofisoprenoidprecursorsinarchaeaandsuggestedthatthisdomainusesanatypicalpathwayofsynthesisoffattyacidsdevoid
ofanyacylcarrierprotein,whichisessentialforthisactivityinbacteriaandeukaryotes.Inaddition,weshowneworupdated
phylogeneticanalysesofenzymeslikelyresponsiblefortheisoprenoidchainsynthesisfromtheirprecursorsandthephospholipid
synthesisfromglycerolphosphate,isoprenoids,andpolarheadgroups.Theseresultssupportthatmostoftheseenzymescanbe
tracedbacktothelastarchaealcommonancestorand,inmanycases,eventothelastcommonancestorofalllivingorganisms.
1.Introduction in diverse archaea [14]; conversely, isoprenoids are known
to be universal although they are synthesized by non-
Archaeawereidentifiedasanindependentdomainoflifein
homologous pathways in the three domains of life, [15];
the late 1970s thanks to the characterization of differences
eventhestereochemistryoftheglycerolphosphatehassome
between their ribosomal RNA molecules and those of
exceptions,asshownbytherecentdiscoveryofarchaeal-like
bacteria and eukaryotes [1]. At that time, it was already
sn-glycerol-1-phosphatespecificlipidsinsomebacteria[16]
known that the so-called “archaeabacteria” held several
andineukaryoticendosomes[17].
atypical biochemical characteristics, of which the most
Today, thanks to the significant accumulation of com-
remarkable was their unusual membrane phospholipids.
plete genome sequence data for a wide variety of species,
Whereas all bacteria and eukaryotes were known to have
it is possible to study the major pathways of phospholipid
membranes based on fatty acids linked by ester bonds to
synthesis and their exceptions by looking at the presence
glycerol-phosphate,archaeaappearedtohavephospholipids
or absence of the corresponding genes in the different
composed of isoprenoid chains condensed with glycerol-
genomes. In addition, these data allows reconstructing the
phosphate by ether linkages [2–6]. Moreover, the archaeal
glycerol ethers contained sn-glycerol-1-phosphate (G1P), evolutionaryhistoryofeachgenebycombiningcomparative
whereasbacterialandeukaryoticonescontainedsn-glycerol- genomics and phylogenetics, namely, by using a phyloge-
3-phosphate(G3P)(forreview,see[7,8]).Thesedifferences, nomic approach. In this paper, we summarize the results
which have been at the center of an intense debate about concerning the phylogenomic studies of the biosynthesis
thenatureofthefirstcellmembranes[9],haveprogressively pathwaysofarchaealphospholipidcomponentsandprovide
been shown to be not so sharp: ether-linked lipids are some new evolutionary data about the enzymes reviewed
common both in eukaryotes (up to 25% of the total lipids in Koga and Morii [18] and Matsumi et al. [19] as likely
in certain animal cells, [10]) and in several thermophilic responsible for the assembly of archaeal lipids from these
bacteria [11–13]; fatty acid phospholipids have been found buildingblocks.
2 Archaea
2.ArchaeaPossessanAtypicalPathwayof andgenerallyrespectingthemainarchaealtaxonomicgroups
BiosynthesisofIsoprenoidPrecursors [31]. These results are consistent with the presence of a
distinctive archaeal MVA pathway in the last archaeal com-
Isoprenoidsarechainsofisopreneunitsandtheirderivatives monancestor(LACA)andsupportthatdifferentisoprenoid
and are found ubiquitously in all living beings. They are precursor biosynthesis pathways are characteristic of each
involved in very diverse functions, such as photosynthetic domainoflife:theclassicalMVApathwayineukaryotes,the
pigments, hormones, quinones acting in electron transport alternativeMVApathwayinarchaea,andtheMEPpathway
chains, plant defense compounds, and so forth [15, 20]. inbacteria.
In archaea, isoprenoids also make up the hydrophobic The origin of the archaeal MVA pathway appears to be
lateral chains of phospholipids [7]. Isoprenoid biosynthesis composite.Theenzymessharedwiththeclassicaleukaryotic
requires two isoprene activated precursors, called isopen- MVApathwaywerealsoancestralineukaryotesandbacteria
tenyl pyrophosphate (IPP) and dimethylallyl diphosphate and, therefore, they can be inferred to have been present
(DMAPP), which act as building parts. The first metabolic in the last common ancestor of all living organisms (the
pathway responsible for the biosynthesis of isoprenoid cenancestor), from which the archaeal lineage would have
precursorswasdiscoveredinyeastsandanimalsinthe1950s inherited them. The last enzymes of the eukaryotic MVA
and named mevalonate (MVA) pathway in reference to its pathwayweremostlikelypresentintherespectiveancestors
first committed precursor. Since its first description, the ofeukaryotesandbacteria,buttheirdistributioninarchaea
MVA pathway was thought to synthesize the isoprenoid isscarceandcomplex:homologuesofMDCcanbedetected
precursorsinallorganisms[20],butcloserscrutinyshowed inHaloarchaeaandThermoplasmatalesandsomeIDI1genes
its absence in most bacteria [21]. An elegant series of have been identified in Haloarchaea and Thaumarchaeota,
multidisciplinary approaches allowed in the late 1990s and although they most likely reflect recent horizontal gene
early2000sdescribinganindependentandnon-homologous transfer (HGT) events from bacterial donors, as deduced
pathwayin bacteria,the methylerythritol phosphate (MEP) from their position well nested among bacterial sequences
pathway(see[22]forreview).TheMEPpathwaywasfound in phylogenetic analyses [23, 31]. In contrast, the class
tobewidespreadinbacteriaandplastid-bearingeukaryotes, Sulfolobales contains PMK and MDC homologues which
whereas the MVA pathway was assumed to operate in robustly branch in an intermediate position between the
archaeaandeukaryotes[15,23].Intheearly2000s,archaeal eukaryoticandthebacterialsequences,suggestingthatthese
isoprenoids were thought to be synthesized through the sequencescouldbeancestralversionsthatwouldhavebeen
MVApathwaybecausethe14C-labelledintermediatesofthis lostintherestofarchaea[31].Ifthisisthecase,aeukaryotic-
pathway were shown to be incorporated into the archaeal like pathway (except for the IDI function, which remains
phospholipids[24].However,onlytwooftheenzymesofthe ambiguous)canbeproposedtohaveexistedinthecenances-
eukaryoticpathwayhavebeendescribedinarchaea[25,26]. tor. This pathway would have been replaced by the MEP
Moreover, the search of MVA pathway enzyme sequences pathway in the bacterial lineage, whereas in archaea only
in archaeal genomes revealed that from the seven enzymes the last steps were replaced by non-homologous enzymes.
acting on this pathway, most archaeal species lack the last We do not know the evolutionary forces that drove these
three of them: phosphomevalonate kinase (PMK), meval- changes;however,themevalonatekinase(MVK),PMK,and
onate diphosphate decarboxylase (MDC), and isopentenyl MDCbelongtoalargefamilyofkinases,namelytheGHMP
diphosphateisomerase(IDI1),involvedintheconversionof kinases [33], which is characterized by a high structural
phosphomevalonate into IPP and DMAPP [27]. Attempts and mechanistic conservation that contrasts with the large
to characterize these missing archaeal enzymes revealed rangeofsubstratesthattheycanuse[34].Ifweassumethat
two new enzymes: the isopentenyl phosphate kinase (IPK) ancestorsoftheseenzymeswerenotveryspecific,thiscould
andanalternativeisopentenyldiphosphateisomerase(IDI2) haveallowedsometolerancetorecruitmentofevolutionary
[28–30].Althoughthedecarboxylationreactionrequiredto unrelated enzymes not only in archaea but also in some
synthesize isopentenyl phosphate from phosphomevalonate eukaryotes that have replaced their ancestral PMK by a
hasnotbeendescribedyet,analternativefinalMVApathway non-homologousone[35,36].Inagreementwiththisidea,
involvingIPKandIDI2wasthenproposedtoexistinarchaea the archaeal IPK itself appears to be able to use different
(Figure1,[29]). substrates [37], which could have made the replacement
Takingadvantageoftherecentaccumulationofgenomic easier.
data,wecarriedoutathoroughphylogenomicanalysisofthe
pathwaysofisoprenoidprecursorsynthesis[31].Concerning
archaea, our presence-and-absence analysis extended the 3.EarlyEvolutionof
presence of the proposed archaeal alternative pathway to IsoprenoidChainSynthesis
a wide archaeal diversity. The main exception to these
observations was Nanoarchaeum equitans, which explains Once the isoprenoid precursors, IPP and DMAPP, have
the dependence of this organism to obtain its lipids from been synthesized, they still have to be assembled to make
itscrenarchaealhost,Ignicoccushospitalis[32].Phylogenetic isoprenoidchains.Theprenyltransferasesresponsibleforthis
reconstructions of the MVA pathway enzymes present in function are the isoprenyl diphosphate synthases (IPPS).
archaeasystematicallyrevealedacladeindependentfromthe Since many more complete genome sequences are now
otherdomainsoflife,representativeofthearchaealdiversity available than at the time of previous IPPS phylogenetic