(Endo)symbiotic Methanogenic Archaea

264 Pages·2018·8.53 MB·English

by  Johannes H. P. Hackstein

Microbiology Monographs
Series Editor: Alexander Steinbüchel
Johannes H. P. Hackstein Editor
(Endo)symbiotic
Methanogenic
Archaea
Second Edition
Microbiology Monographs
Volume 19
SeriesEditor
AlexanderSteinbüchel
Münster,Germany
Moreinformationaboutthisseriesathttp://www.springer.com/series/7171
Johannes H. P. Hackstein
Editor
(Endo)symbiotic
Methanogenic Archaea
Second Edition
Editor
JohannesH.P.Hackstein
IWWR
FacultyofScience
RadboudUniversityNijmegen
Nijmegen,TheNetherlands
ISSN1862-5576 ISSN1862-5584 (electronic)
MicrobiologyMonographs
ISBN978-3-319-98835-1 ISBN978-3-319-98836-8 (eBook)
https://doi.org/10.1007/978-3-319-98836-8
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Preface
Methanogensareprokaryoticmicroorganismsthatproducemethaneasendproduct
of their metabolism. They are strictly anaerobic archaea belonging to the taxon
Euryarchaeota. Methanogens occupy a wide variety of anaerobic environments,
evenextremehabitatscharacterizedbyhightemperature,highsalinity,andextreme
pH(LiuandWhitman2008).Moretemperatehabitatsincludemarineandfreshwater
sediments,floodedsoils,landfills,anaerobicdigesters,geothermalsystems,andthe
heartwoodoftrees.Notably,methanogensalsothriveinthecytoplasmofanaerobic
unicellular eukaryotes and in the gastrointestinal tracts of animals and humans.
Frequently, they attach to the internal surfaces of the gastrointestinal tracts and of
the protists living in intestinal environments with the aid of special adhesion-like
proteins(LiuandWhitman2008).Ininsectguts,methanogenshavetocopewitha
very specialenvironment,since they are exposed toa continuous influx of oxygen
throughthegutwallthatchallengesthestrictlyanaerobicsymbionts.Notwithstand-
ingthatmethanogensareverydiverge,theycanuseonlyaveryrestrictednumberof
substrates.Theyareunabletouseorganicsubstances(withtheexceptionofacetate
and formate), and consequently, methanogens must rely on CO , methyl group
2
containing compounds, and acetate, which are provided by the fermentations
performed by complex anaerobic bacterial communities. The methanogenic sub-
strates are predominantly metabolized with the aid of H that is provided by
2
syntrophic bacterial communities or, in the case of certain anaerobic protists, by
the action of specialized mitochondrion-derived organelles, the hydrogenosomes.
Since both hydrogenosomes and syntrophic bacterial communities rely on a low
concentration of H , the interspecies hydrogen transfer that is mediated by
2
methanogens is crucial for the proper functioning of hydrogenosomes and
syntrophicanaerobicbacterialcommunities.
The synthesis of methane follows a complex biochemical pathway that is char-
acterized by a number of unique coenzymes and membrane-bound enzyme com-
plexes.IthasbeenreviewedthoroughlybyHedderichandWhitman(2006).CO is
2
reduced to methane by H in hydrogenotrophic methanogens, which represent the
2
majority of the methanogens living in symbiosis with protists and multicellular
v
vi Preface
animals.Thesecondtypeofsubstrate,methylgroup-containingcompoundsinclud-
ing methanol, methylated amines, and methylated sulfides, is used by
methylotrophicmethanogens,whicharepredominantlyfoundinthegastrointestinal
tracts of mammals and insects. The third type of substrate is acetate, which is
metabolized by acetoclastic methanogens. Although only two genera
(Methanosarcina and Methanosaeta) use acetate as substrate, as much as
two-thirds of the biologically generated methane is derived from acetate. Notably,
acetoclastic methanogens are rare among the symbiotic methanogens. This is not
surprising since symbiotic acetoclastic methanogens compete with their hosts for
acetate. Notwithstanding, an acetoclastic methanogen has been identified as endo-
symbiontinthefree-livingprotistMetopuses(Narayananetal.2009).
(cid:1)
MethanogensareabundantinhabitatswhereelectronacceptorssuchasO ,NO ,
2 3
Fe3+, and SO 2(cid:1) are limiting (Liu and Whitman 2008). In such methanogenic
4
habitats, complex organic matter is degraded to methane by the syntrophic action
ofdifferentgroupsofanaerobicbacteria.Organicpolymersaredegradedinitiallyby
specialized bacteria to sugars, lactate, short-chain fatty acids, and alcohols. These
products are further fermented by other bacteria to acetate, formate, H , and CO ,
2 2
which are the substrates used by methanogens. These methanogens catalyze the
terminal step in the anaerobic food chain by converting the various methanogenic
substratestomethane,whichisreleasedintotheatmosphere.Morethan70%ofthe
annualglobalmethaneemissions(rangingfrom500to600TgCH /year)stemfrom
4
biologicalmethanogenesisandcontributesignificantlytoglobalwarming(Whitman
etal.2006).Thesymbioticmethanogensinthegastrointestinaltractofruminantsand
other“methanogenic”mammalscontributesignificantlytotheglobalmethanebud-
get.Especiallytherumenhostsanimpressivediversityofmethanogens,whichhave
beenstudiedusingculture-independent16SrRNAmethods(JanssenandKirs2008;
Kittelmann and Janssen 2011; Kittelmann et al. 2013; St-Pierre and Wright 2013;
Wright et al. 2004). Insects, in particular termites, also host very complex
methanogeniccommunities,buttheyreleasemuchlessmethaneduetotheconcom-
itantoxidationofmethaneinthesoilandthetermitemounds.Also,thecontributions
bythemethanogenicendosymbiontsofprotistslivinginfreshwatersedimentscanbe
neglected(vanHoeketal.2006).
This monograph deals with methanogenic endosymbionts of free-living and
symbiotic protists, episymbionts of rumen ciliates, methanogenic endosymbionts
ofciliatesandtermiteflagellates,whicharesometimesaccompaniedbyeubacterial
endosymbionts, and methanogens in the gastrointestinal tract of vertebrates and
arthropods. One review summarizes our knowledge about the genomic conse-
quences of living together in symbiotic associations; another review discusses the
role of methanogens in syntrophic degradation. Finally, the current state of infor-
mationabouthydrogenosomeshasbeenreviewed.
We gratefully acknowledge the efforts of the authors who contributed excellent
chapters to this volume of Microbiology Monographs. We thank Springer for
publishingthismonograph.
Nijmegen,TheNetherlands JohannesH.P.Hackstein
June2018
Preface vii
References
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Contents
Free-LivingProtozoawithEndosymbioticMethanogens. . . . . . . . . . . . 1
TomFenchelandBlandJ.Finlay
AnaerobicCiliatesandTheirMethanogenicEndosymbionts. . . . . . . . . 13
JohannesH.P.HacksteinandRobM.deGraaf
SymbioticMethanogensandRumenCiliates. . . . . . . . . . . . . . . . . . . . . 25
KazunariUshida
MethanogenicandBacterialEndosymbiontsofFree-LivingAnaerobic
Ciliates. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 37
NaoyaShinzato,KazutakaTakeshita,andYoichiKamagata
TermiteGutFlagellatesandTheirMethanogenicandEubacterial
Symbionts. . . . . . . .. . . . . . . . . . . . .. . . . . . . . . . . .. . . . . . . . . . . . .. . 55
YuichiHongohandMoriyaOhkuma
MethanogensintheDigestiveTractofTermites. . . . . . . . . . . . . . . . . . . 81
AndreasBrune
MethanogenicArchaeainHumansandOtherVertebrates:
AnUpdate. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 103
EverlyConwaydeMacarioandAlbertoJ.L.Macario
MethanogensintheGastrointestinalTractofAnimals. . . . . . . . . . . . . . 121
JohannesH.P.HacksteinandTheoA.vanAlen
SyntrophyinMethanogenicDegradation. . . . . . . . . . . . . . . . . . . . . . . . 153
NicolaiMüller,PeerTimmers,CarolineM.Plugge,AlfonsJ.M.Stams,
andBernhardSchink
ix
x Contents
Hydrogenosomes. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 193
JohannesH.P.HacksteinandAloysiusG.M.Tielens
EvolutionofProkaryote-AnimalEndosymbiosisfromaGenomics
Perspective. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 223
RosarioGil,AmparoLatorre,andAndrésMoya
Index. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 257