aerobic ammonia oxidation , the first and rate - limiting step in nitrification , is the only biological process converting reduced to oxidized inorganic nitrogen species on earth . for over 100 years ,
this process was thought to be mediated by autotrophic beta - proteobacteria and gamma - proteobacteria ( aob )   occasionally supported by heterotrophic nitrifiers in soil environments .
however , in situ measurements of nitrification in marine and terrestrial environments showed that ammonia oxidation often proceeds at substrate concentrations significantly below the growth threshold of cultured aob ( e.g. ) indicating the presence of unknown nitrifiers .
the recent discovery of homologs of ammonia monooxygenase genes in archaea [ 57 ] and the cultivation of autotrophic ammonia - oxidizing archaea ( aoa ) [ 811 ] revealed that an additional group of microorganisms is able to catalyze this process .
the widespread distribution of putative archaeal ammonia monooxygenase ( amo ) genes and their numerical dominance over their bacterial counterparts in most marine and terrestrial environments suggested that aoa play a major role in global nitrification [ 1215 ] , but our understanding of their evolutionary history and metabolic repertoire is still in its infancy .
in 1992 , jed fuhrman 's team and ed delong reported the discovery of a novel clade of archaeal 16s rrna sequences from ocean surface waters , which formed a mesophilic sister group to the hyperthermohilic crenarchaeota .
when it became apparent that this novel group contained aoa , these organisms were consequently also referred to as mesophilic crenarchaeota .
this perception was questioned by phylogenetic analysis of the first available genome sequence of a putative aoa , the sponge symbiont candidatus cenarchaeum symbiosum .
when brochier - armanet and colleagues analyzed a concatenated data set of 53 ribosomal proteins common to archaea and eukarya , they made the surprising observation that c. symbiosum branched off before the separation of crenarchaeota and euryarchaeota .
based on this phylogenetic analysis , on gene presence / absence data , and on the diversity and wide distribution of aoa , they proposed that that these organisms belong to the phylum thaumarchaeota .
recently , this analysis was extended to the ammonia - oxidizing candidatus nitrosopumilus maritimus , a marine group i.1a representative , and candidatus nitrososphaera gargensis , a soil group i.1b representative enriched from a hot spring . in this study ,
phylogenetic analysis of concatenated ribosomal proteins ( figure 1a ) and several other marker genes as well as presence / absence patterns of information processing machineries in archaea strongly supported the assignment of aoa to the deep - branching phylum thaumarchaeota .
consistent with this finding , comparative genomics revealed that 6 conserved signature indels and > 250 proteins are unique to the thaumarchaeota c. symbiosum and n. pumilus and are not found in crenarchaeota .
additional support for the phylum thaumarchaeota stems from comparative analysis of fosmid clones obtained from different deep - sea locations . among 200 phylogenetic trees of protein families present in thaumarchaeotal fosmids from these sites , thaumarchaeota sequences branched as separate cluster distinct from hyperthermophilic crenarchaeota and euryarchaeota in 162 phylogenetic trees .
independent from genomic data , the presence of the lipid crenarchaeol in all analyzed aoa [ 9,2224 ] is consistent with a separate placement of these organisms in the archaeal tree as this lipid has so far not been found in any other bacterium or archaeon .
thus , it seems likely that this membrane lipid , which may now be more appropriately termed thaumarchaeol , is an invention of an early thaumarchaote and represents a signature lipid for this phylum . revisiting
the phylogenetic placement of thaumarchaeota in 16s rrna - based trees also reveals a clear separation from crenarchaeota and euryarchaeota ( figure 1b ) . a number of environmentally retrieved clone groups consisting of the sagmgc-1 group ( subsurface mine ) , group i.1c ( acidic soils ) , aloha group ( open ocean ) , psl12 group ( hot spring ) , and the hwcgiii / nitrosocaldus group ( hot springs / hydrothermal vents )
since this cluster is supported by all treeing methods and has a bootstrap value of 100% ( figure 1b ) , its representatives very likely all belong to the phylum thaumarchaeota and at least some of them might be aoa . supporting this hypothesis ,
a good correlation between copy numbers of archaeal amoa ( coding for the -subunit of ammonia monooxygenase ) and 16s rrna genes of the aloha group has been observed in the north pacific .
it will be fascinating to see whether all thaumarchaeota have the capability to perform ammonia oxidation or whether certain members use a different energy metabolism .
just recently two giant thaumarchaeota , candidatus giganthauma karukerense and candidatus giganthauma insulaporcus , were characterized by molecular methods but all attempts to amplify archaeal amoa genes failed . however ,
this could also be caused by primer bias as has been previously recognized for archaeal amoa - targeted surveys in deep ocean waters .
currently , the mcg ( miscellaneous crenarchaeotic group ) , mbgb ( marine benthic group b ) , and hwcgi ( hot water crenarchaeotic group i ) clusters have no clear affiliation to any of the established archaeal phyla and show an unstable branching order when 16s rrna - based trees inferred with different treeing methods are compared ( figure 1b ) .
little is known about these organisms but recently the first genome of a representative of the hwcgi cluster , that of candidatus caldiarchaeum subterraneum , was found to be distinct from other archaeal phyla including genes encoding a ubiquitin - like protein modifier system that was so far only found in eukaryotes . as a consequence , the lineage 
however , a comparative genome analysis by brochier - armanet and colleagues revealed some typical thaumarchaeal features in c. subterraneum and thus places it at the base of thaumarchaeota in protein trees ( for details see brochier - armanet et al .
, this issue ) . with the availability of more genomes within this and related lineages , comparative genomics will show whether 
aigarchaeota represent a new archaeal phylum or will be classified as deep - branching members of the crenarchaeota or thaumarchaeota .
the phylogenetic structure of aoa can also be analyzed by the functional marker gene amoa , which is found in all ammonia - oxidizing microorganisms .
the presence of aoa within group i.1a and group i.1b thaumarchaeota as well as within the thaumarchaeota - group hwcgiii / nitrosocaldus is mirrored in the respective amoa phylogeny ( figure 1b ) .
in addition , a fourth amoa - cluster with no established link to a thaumarchaeotal lineage in the 16s rrna - based tree became apparent during the accumulation of environmental amoa sequences within the last few years .
since amoa sequences from a wide range of habitats ( including various marine , terrestrial , and hot water environments ) are affiliated with this lineage , we have named it the  ubiquitous cluster. it is tempting to speculate that this cluster represents so - far unrecognized aoa within the sagmgc-1 , group i.1c , aloha , or psl12 cluster .
almost every study that investigates ammonia - oxidizing thaumarchaeota uses the amoa gene to explore their diversity and abundance with the implicit assumption that all amoa - carrying archaea are oxidizing ammonia .
however , of the > 10,000 deposited archaeal amoa sequences , thus far only four have been directly linked to archaeal strains for which experimental evidence of ammonia oxidation exists [ 811 ] .
although phylogenetically closely related enzymes often perform the same function , it deserves consideration that the family of copper - containing membrane - bound monooxgenases ( cummo ) , to which archaeal ammonia monooxygenases belong , has a wide substrate range .
in addition to ammonia [ ammonia monooxygenase ( amo ) in -proteobacteria , -proteobacteria , and thaumarchaeota ] , this includes methane [ particulate methane monooxygenase ( pmmo ) in -proteobacteria , -proteobacteria , verucomicrobia , and candidatus methylomirabilis oxyfera ] , and short - chained alkanes [ particulate butane monooxygenase ( pbmo ) in the gram - positive nocardioides strain cf8 ] .
in addition , non - specific substrate catabolism such as oxidation of chlorinated ethenes and aromatic hydrocarbons has been observed with some members of this enzyme family , clearly indicating substrate promiscuity .
therefore , it has been suggested that not necessarily the type of cummo but rather the downstream enzyme machinery defines the energy metabolism of a microorganism . for example , the -proteobacterium aob nitrosococcus oceani can oxidize methane but lacks all subsequent enzymes to gain energy by methane oxidation .
likewise , co - oxidation of ammonia by methane oxidizing bacteria does not support their growth .
furthermore , it is interesting to note that -proteobacterial amos are more closely related to -proteobacterial pmmos than to -proteobacterial amos and have a near equal substrate specificity for ammonia and methane .
consequently , the mere presence of an amoa - like gene , transcript , or protein is insufficient to infer that the respective organism is oxidizing ammonia .
currently , it is not clear whether aoa are strict autotrophs or also assimilate organic substrates . for n. maritimus , autotrophy has been shown   and for n. gargensis co2-fixation has been experimentally demonstrated .
incorporation of labeled bicarbonate into lipids , proteins , and cells of marine thaumarchaeota   are consistent with autotrophy , which is enabled by a modified 3-hydroxypropionate/4-hydroxybutyrate ( hp / hb ) cycle for co2-fixation as found in known aoa genomes and in marine thaumarchaeal fosmids . however ,
analysis of the c. symbiosum and n. maritimus genomes as well as of thaumarchaeal fosmids from bathypelagic plankton also has revealed the presence of a tca cycle ( possibly incomplete ) and of potential transporters for organic substances such as amino acids , oligopeptides , and glycerol .
thus , mixotrophic or even heterotrophic growth of marine thaumarchaeota as supported by other isotope labeling studies and natural distribution of radiocarbon in archaeal membrane lipids   can to date not be excluded .
furthermore , it has been suggested that parts of the hp / hb cycle can serve to co - assimilate organic compounds including , for example , 3-hydroxypropionate , an intermediate in the metabolism of the ubiquitous marine osmoprotectant dimethylsulphoniopropionate . for soil environments ,
co2-stable isotope probing revealed ammonia oxidizing activity of members of group i.1a as well as i.1b thaumarchaeota   indicating an autotrophic or mixotrophic lifestyle .
two of these studies found label incorporation into genes or transcripts of the 4-hydroxybutyryl - coa - dehydratase   or acetyl - coa - propionyl - coa - carboxylase , respectively , with both enzymes being involved in the co2-fixing hp / hb cycle .
however , growth of soil aoa with no concomitant incorporation of co2 has been also observed when nitrification was inhibited   indicating that at least some soil aoa can grow heterotrophically . for comparison , heterotrophic growth of crenarchaeota that possess the hp / hb cycle
is known for sulfolobus solfataricus and metallosphaera sedula with the latter being able to switch between an autotrophic and heterotrophic lifestyle .
the question under which conditions aoa or aob dominate ammonia oxidation is currently attracting a lot of attention . for ammonia oxidation by the group i.1a
thaumarchaeote n. maritimus , an extremely low substrate threshold ( < 10  nm total nh4  +  nh3 , representing the detection limit of the used method ) and apparent km - value ( 133  nm ) were determined with the latter being very similar to in situ nitrification measurements made in oligotrophic oceans .
adaptation to low ammonium concentrations has also been reported for the thermophilic group i.1b thaumarchaeote n. gargensis , indicating a widespread distribution of oligotrophic ammonia oxidation within the thaumarchaeota . in comparison ,
minimum total ammonium concentrations required for growth of cultured aob are 100-fold higher ( > 1  m near neutral ph ) with km - values ranging from 46 to 1780  m total ammonium .
thus , a dominating activity of aoa in the large water bodies of oligotrophic oceans is highly likely with aob being restricted to organic - matter rich particles and coastal environments with higher nutrient loads .
measured apparent km - values for soils range from 2 to 42  m total ammonium   and may therefore be influenced by both aoa and aob . in general , activity of soil aoa
was seen when total ammonia concentrations were below 15  g nh4-n ( g dw .
soil )   whereas aob responded to high ammonia concentrations [ > 100  g  nh4-n ( g dw . 
in addition , the form of supplied nitrogen might also play a critical role : aoa activity was seen when n was supplied as mineralized organic n derived from composted manure or soil organic matter and aob - dominated activity was seen with ammonia from inorganic fertilizer ( reviewed in ) . based on genome analyses of n. maritimus and c. symbiosum and due to the fact that aoa do not contain a homologue of the bacterial hydroxylamine oxidoreductase ,
a mechanism for ammonia oxidation distinctly different from that of aob has been proposed . here
, ammonia is not oxidized via hydroxylamine ( nh2oh ) as in aob but rather via nitroxyl ( hno ) to nitrite , which possibly involves only 0.5 o2 per nh3 oxidized ( proposed by martin klotz ( louisville ) ) .
this hypothesized lower oxygen demand could explain why aoa are found not only in fully areated soils and oxic marine waters but also in suboxic marine waters , sediments , and oxygen - depleted hot springs . in oxygen gradients of marine sediments and in the stratified water body of the black sea different aoa ecotypes
aoa can also be found over a wide range of ph , temperature , salinity , and phosphate concentrations with some aoa being adapted to sulfidic environments , which extends the potential range of aoa niche differentiation to a multitude of environmental factors ( reviewed in ) .
until recently , methanogenic euryarchaeota were the only known archaea of global relevance for element cycling .
this perception changed with the discovery of ammonia - oxidizing archaea , which belong to the newly recognized archaeal phylum thaumarchaeota and contribute significantly to the global n - cycle and c - cycle .
their shear abundance in the ocean ( up to 20% of all bacteria and archaea ) and extremely low substrate threshold for total ammonium provide compelling evidence for their role as dominant ammonia oxidizers in the open ocean , where they also contribute to primary production by their autotrophic ( or possibly partly mixotrophic ) lifestyle . the dominance of aoa over aob in many terrestrial environments can not be so easily explained .
low km - values of unfertilized soils for ammonia oxidation   might point to a contribution of certain aoa ecotypes to nitrification , especially under low ammonia availability . on the other hand ,
it is well possible that some soil thaumarchaeotes use other substrates than ammonia for energy generation and are heterotrophs or that they switch to ammonia oxidation only under certain environmental conditions .
further dissection of the ecological interplay of aoa groups among themselves and with aob is urgently required and might reveal that aoa exhibit a similar type of niche partitioning as found for different nitrite oxidizers . here ,
prefer low nutrient and microoxic sites , with different nitrospira lineages adapted to different nitrite concentrations .
papers of particular interest , published within the period of review , have been highlighted as: of special interest of outstanding interest  of special interest  of outstanding interest
 thaumarchaeota range among the most abundant archaea on earth . 
 initially classified as  
 mesophilic crenarchaeota , comparative genomics has recently revealed that they form a separate and deep - branching phylum within the archaea . 
 this novel phylum comprises in 16s rrna gene trees not only all known archaeal ammonia oxidizers but also several clusters of environmental sequences representing microorganisms with unknown energy metabolism . 
 ecophysiological studies of ammonia - oxidizing thaumarchaeota suggest adaptation to low ammonia concentrations and an autotrophic or possibly mixotrophic lifestyle . extrapolating from the wide substrate range of copper - containing membrane - bound monooxygenases , to which the thaumarchaeal ammonia monooxygenases belong 
 , the use of substrates other than ammonia for generating energy by some members of the thaumarchaeota seems likely . 
Introduction
From mesophilic Crenarchaeota to Thaumarchaeota
Emerging ecophysiology of Thaumarchaeota
Conclusion and outlook
References and recommended reading