(Endo)symbiotic Methanogenic Archaea

245 Pages·2010·4.7 MB·English

by  Tom Fenchel

Microbiology Monographs
Volume 19
Series Editor: Alexander Steinbu¨chel
Mu¨nster,Germany
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HydrogenosomesandMitosomes:
(Endo)symbioticMethanogenicArchaea
MitochondriaofAnaerobicEukaryotes
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Johannes H.P. Hackstein
Editor
(Endo)symbiotic
Methanogenic Archaea
Editor
Dr.JohannesH.P.Hackstein
IWWR
FacultyofScience
RadboudUniversityNijmegen
Heyendaalseweg135
6525AJNijmegen
TheNetherlands
[email protected]
SeriesEditor
ProfessorDr.AlexanderSteinbu¨chel
Institutfu¨rMolekulareMikrobiologieundBiotechnology
Westfa¨lischeWilhelms-Universita¨t
Corrensstr.3
48149Mu¨nster
Germany
[email protected]
ISSN1862-5576 e-ISSN1862-5584
ISBN978-3-642-13614-6 e-ISBN978-3-642-13615-3
DOI10.1007/978-3-642-13615-3
SpringerHeidelbergDordrechtLondonNewYork
LibraryofCongressControlNumber:2010935950
#Springer-VerlagBerlinHeidelberg2010
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Preface
Methanogens are prokaryotic microorganisms that produce methane as an end-
product of their metabolism. They are strictly anaerobic archaea belonging to the
taxon Euryarchaeota. Methanogens occupy a wide variety of anaerobic environ-
ments, even extreme habitats characterized by high temperature, salinity, and
extreme pH (Liu and Whitman 2008). More temperate habitats include marine
and freshwater sediments, flooded soils, landfills, anaerobic digesters, geothermal
systems, and the heartwood of trees. Notably, methanogens also thrive in the
cytoplasm of anaerobic unicellular eukaryotes and in the gastrointestinal tracts of
animalsandhumans.Frequently,theyattachtotheinternalsurfacesofthegastro-
intestinal tracts and of the protists living in intestinal environments with the aid
ofspecialadhesion-likeproteins(LiuandWhitman2008).Ininsectguts,methano-
gens have to cope with a very special environment, since they are exposed to a
continuousinfluxofoxygenthroughthegutwallthatchallengesthestrictlyanaero-
bic symbionts. Notwithstanding that methanogens are very diverse, they can use
only a very restricted number of substrates. They are unable to use organic
substances (with the exception of acetate and formate), and consequently,
methanogens must rely on CO and methyl-group containing compounds and
2
acetate, which are provided by the fermentations performed by complex anaerobic
bacterial communities. The methanogenic substrates are predominantly metabo-
lized with the aid of H that is provided by syntrophic bacterial communities or,
2
in the case of certain anaerobic protists, by the action of specialized mitochondri-
on-derived organelles, the hydrogenosomes. Since both hydrogenosomes and
syntrophic bacterial communities rely on a low concentration of H , the interspe-
2
cies hydrogen transfer that is mediated by methanogens is crucial for the proper
functioning of hydrogenosomes and syntrophic anaerobic bacterial communities.
The synthesis of methane follows a complex biochemical pathway that is
characterized by a number of unique coenzymes and membrane-bound enzyme
complexes.IthasbeenreviewedrecentlybyHedderichandWhitman(2006).CO
2
isreducedtomethanebyH inhydrogenotrophicmethanogens,whichrepresentthe
2
majority of the methanogens living in symbiosis with protists and multicellular
animals. The second type of substrate, methylgroup containing compounds
v
vi Preface
includingmethanol,methylatedamines,andmethylatedsulfides,isusedbymethy-
lotrophicmethanogens,whicharepredominantlyfoundinthegastrointestinaltracts
ofmammalsandinsects.Thethirdtypeofsubstrateisacetate,whichismetabolized
by acetoclastic methanogens. Although only two genera (Methanosarcina and
Methanosaeta) use acetate as substrate, as much as two-thirds of the biologically
generatedmethaneisderivedfromacetate.Notably,acetoclasticmethanogensare
rare among the symbiotic methanogens. This is not surprising since symbiotic
acetoclastic methanogens compete with their hosts for acetate. Notwithstanding,
an acetoclastic methanogen has recently been identified as endosymbiont in the
free-livingprotistMetopuses(Narayananetal.2009).
Methanogens are abundant in habitats where electron acceptors such as O ,
2
NO (cid:1), Fe3+, and SO 2(cid:1) are limiting (Liu and Whitman 2008). In such methano-
3 4
genic habitats, complex organic matter is degraded to methane by the syntrophic
action of different groups of anaerobic bacteria. Organic polymers are degraded
initially by specialized bacteria to sugars, lactate, short-chain fatty acids, and
alcohols.Theseproductsarefurtherfermentedbyotherbacteriatoacetate,formate,
H and CO , which are the substrates used by methanogens. These methanogens
2, 2
catalyze the terminal step in the anaerobic food chain by converting the various
methanogenicsubstrates tomethane,whichisreleasedintothe atmosphere.More
than70%oftheannualglobalmethaneemission(rangingfrom500to600TgCH /
4
year) stem from biological methanogenesis and contribute significantly to global
warming.(Whitmanetal.2006).Thesymbioticmethanogensinthegastrointestinal
tract of ruminants and other “methanogenic” mammals contribute significantly to
the global methane budget. Especially the rumen hosts an impressive diversity of
methanogens,whichhavebeenstudiedusingculture-independent16SrRNAmeth-
ods(JanssenandKirs2008;Wrightetal.2004).Insects,particularlytermites,also
hostverycomplexmethanogeniccommunities,buttheyreleasemuchlessmethane
duetotheconcomitantoxidationofmethaneinthesoilandthetermitemounds.On
the other hand, the contributions by the methanogenic endosymbionts of protists
livinginfreshwatersedimentscanbeneglected(vanHoeketal.2006).
This monograph deals with methanogenic endosymbionts of free-living and
symbiotic protists, episymbionts of rumen ciliates, methanogenic endosymbionts
of ciliates, and termite flagellates, which are accompanied by bacterial endosym-
bionts,andmethanogensinthegastrointestinaltractofvertebratesandarthropods.
Onereviewsummarizesourknowledgeaboutthegenomicconsequencesofliving
together in symbiotic associations; another review discusses the role of methano-
gens in syntrophic degradation. Finally, the current state of information about
hydrogenosomeshasbeenreviewed.
Wegratefullyacknowledgetheeffortsoftheauthorswhocontributedexcellent
chapters to this volume of Microbiology Monographs. We thank Springer for
publishingthismonographandJuttaLindenbornforsupport.
Nijmegen,TheNetherlands JohannesH.P.Hackstein
Mu¨nster,Germany AlexanderSteinbu¨chel
Preface vii
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Contents
Free-LivingProtozoawithEndosymbioticMethanogens ................... 1
TomFenchelandBlandJ.Finlay
AnaerobicCiliatesandTheirMethanogenicEndosymbionts ............. 13
JohannesH.P.Hackstein
SymbioticMethanogensandRumenCiliates ............................... 25
KazunariUshida
TheMethanogenicandEubacterialEndosymbiontsofTrimyema ........ 35
NaoyaShinzatoandYoichiKamagata
TermiteGutFlagellatesandTheirMethanogenic
andEubacterialSymbionts ................................................... 55
YuichiHongohandMoriyaOhkuma
MethanogensintheDigestiveTractofTermites ........................... 81
AndreasBrune
MethanogenicArchaeainHumansandOtherVertebrates .............. 101
EverlyConwaydeMacarioandAlbertoJ.L.Macario
MethanogensintheGastro-IntestinalTractofAnimals .................. 115
JohannesH.P.HacksteinandTheoA.vanAlen
SyntrophyinMethanogenicDegradation .................................. 143
PetraWorm,NicolaiMu¨ller,CarolineM.Plugge,AlfonsJ.M.Stams,
andBernhardSchink
ix