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Complete Nitrification by Nitrospira Bacteria Holger Daims1, Elena V

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ARTICLE doi:10.1038/nature16461 Complete nitrification by Nitrospira bacteria Holger Daims1, Elena V. Lebedeva2, Petra Pjevac1, Ping Han1, Craig Herbold1, Mads Albertsen3, Nico Jehmlich4, Marton Palatinszky1, Julia Vierheilig1, Alexandr Bulaev2, Rasmus H. Kirkegaard3, Martin von Bergen4,5, Thomas Rattei6, Bernd Bendinger7, Per H. Nielsen3 & Michael Wagner1 Nitrification, the oxidation of ammonia via nitrite to nitrate, has always been considered to be a two-step process catalysed by chemolithoautotrophic microorganisms oxidizing either ammonia or nitrite. No known nitrifier carries out both steps, although complete nitrification should be energetically advantageous. This functional separation has puzzled microbiologists for a century. Here we report on the discovery and cultivation of a completely nitrifying bacterium from the genus Nitrospira, a globally distributed group of nitrite oxidizers. The genome of this chemolithoautotrophic organism encodes the pathways both for ammonia and nitrite oxidation, which are concomitantly expressed during growth by ammonia oxidation to nitrate. Genes affiliated with the phylogenetically distinct ammonia monooxygenase and hydroxylamine dehydrogenase genes of Nitrospira are present in many environments and were retrieved on Nitrospira- contigs in new metagenomes from engineered systems. These findings fundamentally change our picture of nitrification and point to completely nitrifying Nitrospira as key components of nitrogen-cycling microbial communities. Nitrification is catalysed by ammonia-oxidizing bacteria (AOB)1 The globally distributed genus Nitrospira represents the most or archaea (AOA)2 and nitrite-oxidizing bacteria (NOB)1. Since diverse known group of NOB. Nitrospira members have been found the pioneering studies by Winogradsky more than a century ago3, in terrestrial8 and limnic habitats9,10, marine waters11, deep sea nitrifying microorganisms are generally perceived as specialized sediments, sponge tissue12, geothermal springs13, drinking water chemolithoautotrophs that obtain energy for growth by oxidizing distribution systems14, corroded iron pipes15, and wastewater treat- either ammonia or nitrite. The known ammonia-oxidizing microbes ment plants (WWTPs)10,16. At least six phylogenetic sublineages of (AOM) and NOB are phylogenetically not closely related, and none Nitrospira exist, of which lineage II seems to be most widely distrib- of these organisms can oxidize both substrates. This separation of the uted in both natural and engineered ecosystems10. The ecological suc- two nitrification steps in different organisms leads to a tight cross- cess of Nitrospira has been linked to an economical pathway for nitrite feeding interaction and the frequently observed co-aggregation of oxidation17 and a substantial metabolic versatility, which includes AOM with NOB in nitrifying consortia4. However, the functional the utilization of various organic compounds in addition to nitrite 10,11,17–19 separation is a puzzling phenomenon since complete nitrification and CO2 , cyanate or urea degradation and nitrification by −1 19,20 would yield more energy (∆G°′ = −349 kJ mol NH3) than either reciprocal feeding with AOM , and chemolithoautotrophic aerobic −1 21 single step (∆G°′ = −275 kJ mol NH3 for ammonia oxidation hydrogen oxidation . −1 − to nitrite and ∆G°′ = −74 kJ mol NO2 for nitrite oxidation to nitrate). Thus, an organism catalysing complete nitrification should Enrichment of conspicuous Nitrospira have growth advantages over the ‘incomplete’ AOM and NOB. Based A microbial biofilm developing on the walls of a pipe under the flow on kinetic theory of optimal pathway length5,6, Costa et al.7 argued of hot water (56 °C, pH 7.5) raised from a 1,200 m deep oil exploration that a hypothetical complete nitrifier would likely be outcompeted well (Aushiger, North Caucasus, Russia) was sampled and incubated by incomplete, cross-feeding AOM and NOB in many environments. at 46 °C in ammonium-containing mineral medium to enrich mod- However, the same authors7 also pointed out that a complete nitrifier erately thermophilic AOM. After a series of subcultivation steps, we might be competitive under conditions that favour the maximiza- obtained enrichment culture ‘ENR4’ that oxidized ammonia to nitrate tion of growth yield rather than growth rate and coined the term and contained a dense population of cells morphologically resem- “comammox” (complete ammonia oxidizer) to describe such a bling described Nitrospira species13,15 (Extended Data Fig. 1a, b). hypothetical microbe. Conditions selecting for comammox may A second abundant population consisted of rod-shaped cells, but be characterized by slow, substrate-influx-limited growth with a no organism in ENR4 displayed the typical morphologies of known spatial clustering of biomass in microbial aggregates and biofilms7. AOM. Inspection by fluorescence in situ hybridization (FISH) with A prerequisite for the existence of comammox would also be that any nitrifier-specific ribosomal RNA-targeted probes10,22 confirmed that biochemical incompatibilities of ammonia and nitrite oxidation can ENR4 contained Nitrospira (Extended Data Fig. 1c) but no other be overcome by adaptations of enzymes or cellular compartmentali- detectable nitrifiers. Moreover, known bacterial or archaeal genes zation7. Aside from these theoretical considerations, the old question of ammonia monooxygenase (AMO) subunit alpha (amoA) and 16S of whether comammox exists in nature has not been resolved. rRNA genes of AOA were not detected by PCR in ENR4. Considering 1Department of Microbiology and Ecosystem Science, Division of Microbial Ecology, University of Vienna, Althanstrasse 14, 1090 Vienna, Austria. 2Winogradsky Institute of Microbiology, Research Center of Biotechnology of the Russian Academy of Sciences, Leninsky Ave. 33, bld. 2, 119071 Moscow, Russia. 3Center for Microbial Communities, Department of Chemistry and Bioscience, Aalborg University, Fredrik Bajers Vej 7H, 9220 Aalborg, Denmark. 4Helmholtz-Centre for Environmental Research - UFZ, Department of Proteomics, Permoserstrasse 15, 04318 Leipzig, Germany. 5Helmholtz-Centre for Environmental Research - UFZ, Department of Metabolomics, Permoserstrasse 15, 04318 Leipzig, Germany. 6Department of Microbiology and Ecosystem Science, Division of Computational Systems Biology, University of Vienna, Althanstrasse 14, 1090 Vienna, Austria. 7DVGW-Forschungsstelle TUHH, Hamburg University of Technology, Am Schwarzenberg-Campus 3, 21073 Hamburg, Germany. 504 | NATURE | VOL 528 | 24/31 DECEMBER 2015 © 2015 Macmillan Publishers Limited. All rights reserved ARTICLE RESEARCH amo hao s nxr to 36.4) ) ) ) 0 .9 c biogenesi 32. to 67 CcmI (46.6 to 55.7 (57.1 to 67.7 in Ca. Nitrospira Cytochrome Hypothetical Putative transposaseAmoC1AmoA (42.4s clade AmoBto 67.6) A (42.3 (43.3 to OrfMto 60.5) 60.8) (58.4 toCopD 67.2) (27.2CopC to AmoD253.6(28.6AmoD1) to (37.158.7)AmoE1 (31.6 to 47.6) (40.0 to 61.1) toHypothetical 50.3) Hypothetical proteinCycB proteinCycA (53.8HaoB to (40.4 70.6HAO to 47.3 (52.2) prote CcmH ( HypotheticalHypotheticalHypothetical proteins protein proteinPutativePutative transposas transposaseNxrBe NxrA tRNA glycine proteins inopinata MBR Nitrospira bin 1 2 8 3 7 0 3 8 2 93. 82. 85. 53. 95. 85. 98. 87. WWTP VetMed Nitrospira bin 2 8 4 1 9 8 4 0 3 8 3 93. 82. 63. 91. 81. 56. 52. 95. 85. 98. 87. 1 5 0 86. 96. 92. GWW Nitrospira bin 3 5 6 8 3 2 8 3 5 8 2 1 6 3 9 5 7 *55. 59. 84. 80. 55. 73. 73. 61. 69. 60. 90. 82. 99. 93. 40. 49. GWW Nitrospira bin 4 2 7 2 3 6 8 6 0 9 1 0 *55. 61. 82. 80. 55. 72. 68. 59. 64. 98. 98. GWW Nitrospira bin 5 3 3 7 0 2 2 0 6 8 *56. 61. 90. 83. 52. 73. 68. 72. 96. 1 7 90. 80. GWW Nitrospira bin 8 4 9 1 9 9 81. *55. 60. 97. 89. 8 1 8 6 57. 90. 79. 98. GWW Nitrospira bin 9 0 8 3 6 9 2 9 9 8 1 2 3 7 97. 90. 82. 68. 61. 90. 83. 50. 72. 68. 73. 99. 95. 1 99. GWW Nitrospira bin 10 7 1 9 3 1 3 3 0 3 0 88. 81. 66. 63. 89. 84. 51. 73. 99. 97. Figure 1 | Key nitrification gene loci in Ca. N. inopinata and the the predicted gene products compared to Ca. N. inopinata. Asterisks metagenomic Nitrospira population genome bins containing putative mark comammox clade B amoA genes. Wiggly lines indicate ends of comammox Nitrospira. Gene alignments of the amoCAB, hao, and metagenomic contigs. Underlined gene products of Ca. N. inopinata have nxrAB loci with flanking genes are shown. Only two or three of up to homologues in AOB genomes (amino acid identities in per cent to AOB nine syntenic cytochrome c biogenesis genes upstream of the hao loci are are indicated in parentheses), but gene arrangements can differ from displayed. Colours identify homologous genes. Genes without homologues AOB24. Genes and noncoding regions are drawn to scale. Metagenomic in the analysed data set are white if their function is known, otherwise bins are numbered as in Supplementary Table 8. MBR, membrane grey. Transposases are magenta irrespectively of homology. Numbers bioreactor; WWTP, wastewater treatment plant; GWW, groundwater well. below genes represent amino acid sequence identities (in per cent) of the intriguing possibility that the Nitrospira population might be Nitrospira strain as ‘Candidatus Nitrospira inopinata’ (in.o.pi.na'ta. L. responsible for both ammonia and nitrite oxidation, we sequenced fem. adj. inopinata unexpected, surprising). the metagenome of the enrichment (Supplementary Tables 1–7) to identify the ammonia oxidizer. Sequence assembly and differential Discovery of comammox coverage binning23 showed that the ENR4 metagenome was domi- The obtained bacterial genomes were screened for the key functional nated by two organisms (one Nitrospira strain and a betaproteobac- genes of autotrophic nitrification. As expected, Ca. N. inopinata pos- terium affiliated with the family Hydrogenophilaceae) and revealed sesses the key enzyme for nitrite oxidation, nitrite oxidoreductase two additional rare populations (an alphaproteobacterium related to (NXR). Its genome contains the nxrA and nxrB genes coding for the Tepidamorphus gemmatus, family Rhodobiaceae, and an actinobacte- subunits alpha and beta, respectively, of the periplasmic Nitrospira rium affiliated with Thermoleophilum, family Thermoleophilaceae).
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