microbial communities of acidic wetlands are responsible for emissions of the potent greenhouse gases methane ( ch4 ) , and nitrous oxide ( n2o ; conrad , 1996 ; whalen , 2005 ; denman et al . , 2007 ) .
the largest single global source of atmospheric ch4 ( 100237  gt  year ) are acidic wetlands , such as peat bogs and fens that cover 3.5% of the terrestrial surface , but store about 30% of global carbon of terrestrial ecosystems ( gore , 1983 ; denman et al . , 2007 ) .
largest sources of atmospheric n2o are soils under natural vegetation and agricultural use ; nonetheless , certain acidic wetlands that have a high nitrogen content were recently identified as significant sources of n2o displaying n2o emissions in the range of those observed for agricultural soils ( denman et al .
conservative estimates suggest that 0.6% of the global annual emission of n2o might be attributed to such acidic wetlands ( repo et al . , 2009 ) .
acidic wetlands are covered by water - adapted vascular plants , and mosses of the genus sphagnum ( gorham , 1991 ) .
microbes that produce ch4 are methanogenic archaea , and those that are the main source of n2o are denitrifiers in anoxic habitats like wetlands ( conrad , 1996 ; ferry , 1999 ; drake et al . , 2009 ) .
ch4 produced by methanogens is further oxidized by aerobic methanotrophs , which thrive as a significant part of wetland microbial communities and mitigate the net ch4 flux into the atmosphere ( hanson and hanson , 1996 ; shannon et al .
, 1996 ; whalen , 2005 ; knorr et al . , 2008 ; hornibrook et al . , 2009 )
atmospheric oxygen may penetrate soil due to water table draw downs , and gas transport through the aerenchyma of vascular plants into the rhizosphere ( moog and bruggemann , 1998 ; kettunen et al .
, 1999 ; mainiero and kazda , 2005 ; paul et al . , 2006 ) .
acidic wetlands may temporarily turn into sinks of atmospheric ch4 , or at least have the potential to consume atmospheric ch4 ( 1.75  ppmv ; table 1 ; whalen and reeburgh , 2000 ; jauhiainen et al .
, 2005 ; elberling et al . , 2011 ) , a fact that is currently underappreciated , and poorly understood on the level of microbial communities .
acidic wetlands exhibiting consumption of atmospheric ch4 or n2o , and associated methanotroph and denitrifier communities if such data were available .
calculated based on reported first order rate constant ( i.e. , 0.03  h  gsoil dw ) at 1.8  ppmv ( assumption : water content 50% , 1.8  ppmv  =  2.5  nm ; thus , dissolved ch4 concentration is 5  pmol  gsoil dw ) .
this rates are calculated from first order rate constants of ch4 consumption ( i.e. , based on km [ 43  nm ; or 3.6  nmol  gsoil wet weight ] and vmax [ 38.5  nmol  gsoil wet weight ] values as reported in the reference ) at a headspace concentration of 1.8  ppmv .
association of denitrifiers with n2o production in nitrogen - rich acidic wetlands is indicated by process - orientated studies of water - logged acidic soils , and denitrification is suggested as the primary n2o producing process in such systems where the water filled pore space exceeds 70% ( davidson , 1991 ) .
denitrifiers catalyze the sequential reduction of n - oxides to nitrous oxide ( n2o ) and/or dinitrogen ( n2 ) via the sequential action of nitrate , nitrite , nitric oxide , and nitrous oxide reductases ( zumft , 1997 ) .
subunits that contain the catalytic center are encoded by narg / napa , nirk / nirs , norb , and nosz .
dissimilatory reduction of nitrate via nitrite to ammonium ( dnra ) might produce n2o under oxygen limited conditions via the unspecific interaction of nitrite with nitrate reductase ( smith and zimmermann , 1981 ; smith , 1983 ) .
however , dnra potentials are low in acidic wetland soils , and free nitrite is virtually absent from such soils , suggesting that dnra is negligible with regards to n2o production ( anderson and leine , 1986 ; bowden , 1987 ) .
significant products of chemodenitrification are no and no2 rather than n2o ( van cleemput , 1998 ; kappelmeyer et al . , 2003 ; kresovic et al . , 2009 )
n2o is also produced as a by - product during the aerobic conversion of ammonia to nitrate by nitrifiers , but nitrification is the primary source of n2o in oxic rather than water - logged soils ( davidson , 1991 ; conrad , 1996 ) . despite the importance of denitrifiers for n2o production in water - logged soils and the wealth of information on denitrifiers of agricultural and ph - neutral upland soils , studies addressing acid - tolerant denitrifiers in acidic wetlands are just emerging and under - represented in current literature .
evidence is accumulating that soils including acidic wetlands can act as temporary sinks for n2o ( inubushi et al .
, 2003 ; hadi et al . , 2005 ; chapuis - lardy et al . , 2007
indeed , negative fluxes of up to 1.7  mol  n2o  m  h were observed in situ for acidic wetlands ( table 1 ) .
thus , the review intents to delineate the current understanding of microbial communities in acidic wetlands for ch4 and n2o consumption and to highlight research needs .
ch4 fluxes of acidic wetlands are highly variable due to non - linear interactions of environmental factors that control methanogenesis , methanotrophy , and ch4 gas transport ( whalen , 2005 ; spahni et al . , 2011 ) .
one reason of high spatial and temporal variability of ch4 exchange with the atmosphere might be a mitigation of net flux by consumption of atmospheric ch4 ( wieczorek et al . , 2011 ) .
hot spots of activity of methanotrophs in acidic wetlands are anoxic  oxic interfaces , where ch4 and oxygen gradients overlap ( sundh et al . , 1995 ; kettunen et al . , 1999
thus changes in oxygen availability alter both ch4 consumption , and production , and hence , reduce or increase net flux of ch4 from soil into the atmosphere ( kettunen et al . , 1999 ;
total cell numbers of methanotrophs of acidic wetlands range from 10 to 10 cells per gram of wet weight ( sundh et al .
, 1995 ; dedysh et al . , 2001 , 2003 ; dedysh , 2002 , 2009 ; belova et al . , 2011 ) .
methanotrophic pure cultures have primarily been isolated from sphagnum - covered wetlands , and are acid - tolerant strains of methylocystis ( methylocystaceae ) , methylocella , and methylocapsa ( both beijerinckiaceae ; dedysh et al . , 2001 , 2003 ; dedysh , 2002 , 2009 ; kip et al . ,
methylocella species , and some species of methylocystis and methylocapsa utilize also simple multicarbon compounds , such as acetate ( dedysh et al . , 2005 ; theisen et al . , 2005 ; dunfield et al . , 2010 ; belova et al . ,
fluctuations of soil - internal methanogenesis may be caused by varying exudation of plants and redox conditions due to water table changes that can be consequences of drought periods , or heavy rainfall ( knorr et al .
, 2008 ; knorr and blodau , 2009 , dorodnikov et al . , 2011 ) .
methylocystis strain h2s apparently represents a key methanotroph in acidic wetlands ( belova et al . , 2011 ;
strain h2s - related 16s rrna genes ubiquitously occur in northern wetlands , and contribute with 1858% ( i.e. , 0.4    10 to 3.4    10  cells  g of wet weight ) to the alphaproteobacterial methanotrophs in such wetlands ( belova et al . ,
uncultivated species that are phylogenetically related to methylocystis , and methylocapsa are associated with hyaline cells of submerged mosses of sphagnum .
these sphagnum methanotroph associations have been found in various northern wetlands ( kip et al . , 2010 ) .
methanotrophs apparently contribute up to 30% to carbon assimilation of the moss ( raghoebarsing et al .
the association is , based on current observations , not specific since different methanotroph - free sphagnum species can be colonized by methanotrophs that were provided from the same sphagnum individual ( larmola et al . , 2010 ) .
the physiological basis of the interaction between methanotroph and moss has not been fully resolved .
wetland methanotroph communities are usually dominated by alphaproteobacteria , but gammaproteobacterial methanotrophs may also be present ( morris et al . , 2002 ; chen et al .
some of them ( methylomonas- , methylosoma - related strains ) have been isolated , which represent the first acid - tolerant members of the methylococcaceae ( kip et al . , 2011 ) .
all cultured methanotrophs of acidic wetlands are acid - tolerant and have growth optima below ph6 ( dedysh , 2009 ; kip et al . , 2011 ) .
most information on the identities and physiologies of methanotrophs of acidic wetlands are derived from sphagnum - associated microbial communities , but there is a lack of information on vascular plant - associated methanotrophs in acidic wetlands .
acidic wetlands may temporally turn into net sinks of atmospheric ch4 , which has been documented in various studies , or have the capability to utilize atmospheric ch4 concentrations ( table 1 ; figure 1 ; dedysh and panikov , 1997 ; kettunen et al .
, 1999 ; whalen and reeburgh , 2000 ; jauhiainen et al . , 2005 ; elberling et al . , 2011 ; wieczorek et al . ,
many wetland sites have annual emission rates of less than 3.8  mol  ch4  ha  year ( dalal and allen , 2008 ) indicating not necessarily only low ch4 production , but also a certain proportion of consumption of atmospheric ch4 over the year .
proposed model of microbes that are responsible of atmospheric sink function of ch4 and n2o in natural wetlands .
the quantitative contribution to global net fluxes of ch4 and n2o into the atmosphere has not been evaluated in acidic wetlands .
( a ) acidic wetland covered by sphagnum plants with low nitrogen input and mineralization rates .
white pathway : plant - derived organic matter is degraded by microbial fermentation , acetogenesis , and methanogenesis to ch4 that is transported to oxygen - saturated zones close to the surface .
the thickness of the oxygen - saturated layer is dependent of water table level ( white dotted line ) .
methanotrophs ( such as methylocystyceae , beijerinkiaceae , but as well methylococcaceae ) consume up to 90% of methanogenic ch4 .
methanotrophs convert ch4 to carbon dioxide ( co2 ) which is released into the atmosphere .
yellow pathway : methylocystis species likely consume atmospheric ch4 when ch4 supply from anoxic zones is limited .
( b ) natural wetland with high nitrogen input and mineralization rates ( e.g. , minerotrophic fens , palsa peats ) .
white pathway : in nitrogen - rich acidic wetlands ( e.g. , palsa peats ) a part of anaerobic organic matter degradation intermediates are consumed by denitrifiers that reduce no3- to n2o and n2 .
ammonia - oxidizing bacteria ( aob ) are known to produce small amounts of n2o during oxidation of ammonia ( schmidt et al . , 2004 ; braker and conrad , 2011 ) .
yellow pathway : under as - yet unresolved environmental conditions atmospheric n2o may be further reduced to n2 by to date not cultured denitrifiers that use electrons from organic matter .
a very limited number of studies analyzed the composition of methanotroph communities of acidic wetlands , and measured the potential of the respective wetland to consume atmospheric ch4 ( table 1 ) .
methylocystis species that were frequently detected in acidic wetlands are closely related to the solely known methanotroph strains that are capable of consumption of atmospheric ch4 , i.e. , strains lr1 , sc2 , and dwt ( dunfield et al . , 1999 , 2002 ; kolb et al . , 2005 ; baani and liesack , 2008 ; dedysh , 2009 ; wieczorek et al . ,
2011 ) . nonetheless , pmoa2 genes ( that encode for the hydroxylase subunit of a high affinity ch4 mono - oxygenase ) that would indicate the capability of consumption of atmospheric ch4 ( dunfield et al . , 2002 ; yimga et al . , 2003 ; ricke et al . , 2004 ; baani and liesack , 2008 ) have only been detected at low relative abundances ( < 5% ; wieczorek et al . , 2011 ) .
to warrant consumption of atmospheric ch4 in wetlands a small fraction ( about 10 cells per gram dry weight in forest soils that consume atmospheric ch4 ; kolb et al .
2010 ) of the total cell number of present methanotrophs ( about 10 cells per gram dry weight ) need presumably be active to allow for consumption of atmospheric ch4 at rates that were observed in acidic wetland sites .
the major proportion of detectable pmoa ( encodes the beta - subunit of a low affinity membrane bound ch4 mono - oxygenase ) and mmox ( encodes the hydroxylase subunit of a low affinity cytoplasmic bound ch4 mono - oxygenase ) genes in an acidic wetland soil that exhibited the capability of consumption of atmospheric levels of ch4 ( i.e. , 82 and 64% , respectively ) , affiliated with genes of methylocystis ( wieczorek et al . , 2011 ) .
the abundant methylocystis strain h2s harbors as well pmoa2 indicating that this methanotroph may consume atmospheric ch4 ( dedysh , personal communication ) .
thus , methylocystis species of acidic wetlands likely are capable of atmospheric ch4 consumption ( figure 1 ) , and may have the advantage to survive more likely periods of ch4 deficiency , may be periodically the case in minerotrophic fens , and at oxygen - saturated surface - near soil layers .
( ettwig et al . , 2010 ) have not been detected in acidic wetlands . in summary ,
the role of other methanotrophs in acidic wetlands ( i.e. , beijerinckiaceae , and methylococcaceae ) in consumption of atmospheric ch4 is not fully unresolved , but not very likely based on their low affinities for ch4 .
it is not likely that  m. oxyfera  is involved in n2o cycling since it lacks nitric oxide reductase .
one of the most remarkable features of denitrifiers is their capacity to produce and consume n2o ( table 1 ; figure 1 ; zumft , 1997 ) .
such organisms are widely distributed in various environments and highly diverse ( e.g. , zumft , 1997 ; braker and conrad , 2011 ) .
not all denitrifiers known to date are capable of n2o consumption ( zumft and kroneck , 2007 )
. however , n2o is a common intermediate during denitrification and serves as sole electron acceptor for supporting growth of many denitrifiers ( zumft , 1997 ; strohm et al . , 2007 ) .
dna based stable isotope probing with c - labeled succinate as electron donor and n2o as electron acceptor and cultivation - based studies demonstrated growth of putative denitrifiers by n2o reduction in rice field soil ( ishii et al . , 2011 ) .
these findings are in line with a g0 of n2o reduction to n2 that approximates 340  kj  mol under standard conditions , indicating a highly exergonic process ( zumft and kroneck , 2007 ) .
thus , it might not be surprising that n2o consumption by soil communities is a more common phenomenon than previously thought ( table 1 ; reviewed in holtan - hartwig et al .
n2o reductases of denitrifiers catalyze the efficient reduction of n2o to n2 and are copper - dependent metallo - enzymes that exhibit km values in the lower micromolar range for n2o , highlighting the potential of denitrifiers to consume low concentrations of n2o ( zumft , 1997 ) .
abiotic conversion of n2o at ambient temperatures might occur with ( reduced ) transition - metal complexes ( which occur in the active site of n2o converting enzymes ) and metal amides ( banks et al .
metallo - enzymes like carbon monoxide dehydrogenase and cobalamin - dependent methionine synthase are also capable of reducing n2o to n2 , while nitrogenase converts n2o to nh3 ; bacterial nitrite cytochrome c reductase transforms n2o to an unknown product ( jensen and burris , 1986 ; bannerjee and matthews , 1990 ; lu and ragsdale , 1991 ; drummond and matthews , 1994 ; stach et al . , 2000 ) .
such enzymes are hosted by diverse organisms including non - denitrifiers ( see references in zumft , 1997 ; zumft and kroneck , 2007 ) . however , the conversion of n2o by these aforementioned enzymes is regarded as a non - physiological reaction . low km values and high specific activities for n2o ( as were demonstrated for n2o reductases of denitrifiers ) have not been demonstrated for such enzymes , suggesting a minor role , if any , for the consumption of atmospheric n2o concentrations ( 319  ppb , equivalent to app . 8  nmol n2o per liter soil solution ; conrad , 1996 ) in soils ( zumft , 1997 ; stach et al . , 2000 ; zumft and kroneck , 2007 ) .
in this context , dissimilatory reducers of nitrate producing ammonia of the enterobacteriaceae that were shown to consume n2o in the laboratory displayed a km value of 3  mm for n2o , likewise suggesting that the n2o reduction is a non - physiological reaction and probably of minor importance in situ ( kaldorf et al .
moreover , assimilatory reduction of n2o that might theoretically proceed via nitrogenase action was not detected in soils ( vieten et al . , 2008 ) .
thus , denitrifiers hosting n2o reductases deserve primary attention in the context of n2o consumption in soils .
denitrification rates and the ratio of n2o to total nitrogen gas products are regulated by oxygen availability , ph , temperature , carbon to nitrogen ratio , the availability of substrates , and electron acceptors , as well as by the denitrifier community composition ( van cleemput , 1998 ; drsch et al . , 2011 ) .
anoxia ( as indicated by a water filled pore space of greater than 60% ) , a carbon to nitrogen ratio greater than 30 , and ph - neutral conditions favor complete denitrification to n2 in soils including acidic wetlands ( conrad , 1995 , 1996 ; klemedtsson et al . , 2005 ;
cuhel et al . , 2010 ; braker and conrad , 2011 ) . a ph value below 5 is often encountered in peatlands , and is hypothesized to impair n2o reduction and to increase the product ratio of n2o to n2 ( simek and cooper , 2002 ; cuhel et al . , 2010 )
. however , acidic wetlands host acid - tolerant denitrifiers capable of n2o reduction and complete denitrification ( palmer et al . , 2010 , 2011 ) .
moreover , evidence of active denitrification - associated n2o production and consumption , ( including consumption of atmospheric n2o concentrations ) was obtained by compound specific stable isotope analyses of n2o in one acidic wetland ( goldberg et al . , 2008 , 2010 ) .
in that specific wetland , n values indicated that n2o produced in deep soil layers was partially consumed upon its diffusion to the soil surface ( goldberg et al .
, 2008 , 2010 ) , suggesting that denitrifiers might contribute to the mitigation of n2o emission from acidic wetlands .
denitrifiers that exhibit the genetic potential to consume n2o were detected in acidic wetlands by the analysis of nosz genes .
detected nosz genes in acidic wetlands mostly affiliated with nosz from uncultured soil bacteria or were only distantly related to known genes , suggesting a wealth of uncultured denitrifier diversity in acidic wetlands ( palmer et al .
phylogenies of nosz and 16s rrna genes from the same organisms are basically congruent ( jones et al .
, 2008 ; palmer et al . , 2009 ) , allowing to speculate on the identity of organisms hosting the detected nosz .
thus , putative n2o reducers in acidic wetlands include alphaproteobacteria ( azospirillum , brady- , and mesorhizobium ) , betaproteobacteria ( achromobacter , ralstonia ) , and gammaproteobacteria ( pseudomonas ) .
however , it remains to be determined whether the detected n2o reductase genes were expressed , i.e. , the detected organisms reduce n2o in situ ( figure 1 ) .
analyses of other genes associated with denitrification corroborate that acidic wetlands harbor diverse and new denitrifiers ( palmer et al . , 2010 , 2011 ) .
however , given the low number of studies addressing n2o - consuming denitrifier communities in acidic wetlands , and the selectivity of pcr - based gene marker analyses , the present studies have to be regarded as providing a minimal estimate of denitrifier diversity capable of n2o consumption ( throback et al .
, 2004 ; green et al . , 2010 ; heylen et al . , 2011 ; jones et al . , 2011 ) .
the fact that high affinity respiratory n2o reduction occurs in non - denitrifying organisms that reduce nitrate but lack nitrite reductase activity , and that nitrifiers were shown to have the capability to consume n2o and produce n2 further complicates matters ( yoshinari , 1980 ; mcewan et al . , 1985 ; zumft , 1997 ; schmidt et al . , 2004 ) .
nevertheless , the relevance of n2o consumption for mitigation of n2o emissions , and eventually a temporary sink function of acidic wetlands for n2o is emerging , although the physiology and taxonomic identity of  microbial catalysts  have not been sufficiently resolved .
furthermore , the regulation of n2o reduction in situ and on cellular level , and thus the potential of the soil to reduce n2o to n2 , and the diffusivity of n2o within the soil profile will impact the sink functions of wetland soils for n2o but are likewise only poorly resolved .
few studies addressed the role of methanotrophs and denitrifiers in consumption of atmospheric ch4 and n2o in acidic wetlands .
potential consumption activities have been measured in laboratory - scale experiments , and first evidence for denitrification - associated n2o consumption in situ is available .
systematic in situ flux measurements combined with measurements of environmental parameters , consumption potentials , stable isotope signatures of carbon and nitrogen in ch4 and n2o pools , and community analyses are needed to improve our understanding of environmental factors that trigger ch4 and n2o consumption in acidic wetland soils .
the authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest .
 acidic wetlands are global sources of the atmospheric greenhouse gases methane ( ch4 ) , and nitrous oxide ( n2o ) . 
 consumption of both atmospheric gases has been observed in various acidic wetlands , but information on the microbial mechanisms underlying these phenomena is scarce . 
 a substantial amount of ch4 is consumed in sub soil by aerobic methanotrophs at anoxic  oxic interfaces ( e.g. , tissues of sphagnum mosses , rhizosphere of vascular plant roots ) . 
 methylocystis - related species are likely candidates that are involved in the consumption of atmospheric ch4 in acidic wetlands . 
 oxygen availability regulates the activity of methanotrophs of acidic wetlands . 
 other parameters impacting on the methanotroph - mediated ch4 consumption have not been systematically evaluated . 
 n2o is produced and consumed by microbial denitrification , thus rendering acidic wetlands as temporary sources or sinks for n2o . 
 denitrifier communities in such ecosystems are diverse , and largely uncultured and/or new , and environmental factors that control their consumption activity are unresolved . analyses of the composition of n2o reductase genes in acidic wetlands suggest that acid - tolerant proteobacteria have the potential to mediate n2o consumption in such soils . 
 thus , the fragmented current state of knowledge raises open questions concerning methanotrophs and denitrifiers that consume atmospheric ch4 and n2o in acidic wetlands . 
Introduction
Methanotrophs of Acidic Wetlands
Specialized Methanotrophs Mediate CH
Do Denitrifiers Consume N
Future Perspectives
Conflict of Interest Statement