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Supporting Information Supporting Information Koch et al. 10.1073/pnas.1506533112 SI Results and Discussion transporters may facilitate the uptake of one or more of the tested Urea Transport and Accessory Proteins of Urease in N. moscoviensis. organics. However, no nitrate reduction was observed during Urea is a small uncharged molecule that diffuses readily through anoxic incubations with any of these substrates (Fig. S4B). the lipid bilayers of bacterial membranes (52). Aside from passive Nitrospira diffusion, the transport of urea into bacterial cells is mediated by Core Metabolism of for Chemolithoautotrophic Nitrite urea-specific channels such as UreI of Helicobacter (53) or by ATP- Oxidation. A syntenic gene arrangement is conserved in rela- dependent ABC transporters such as UrtABCDE in Cyanobacteria tively large parts of the N. moscoviensis and N. defluvii genomes (54). ABC transporters for urea consist of a periplasmic substrate- (Fig. S7A). Shared genomic features with a highly conserved binding protein (UrtA), a dimer of the transmembrane proteins synteny are the enzymatic repertoire for nitrite oxidation, the electron transport chains for aerobic respiration and reverse UrtB and UrtC, which form a membrane-crossing pore, and the + ATP-binding and -hydrolyzing proteins UrtD and UrtE (54, 55). electron transport from nitrite to NAD , and the reductive tri- These ABC transporters show a high affinity for urea (52, 54) and carboxylic acid (rTCA) cycle for CO2 fixation and the oxidative – may represent an adaptation to environments with urea concen- TCA cycle (Fig. S7 B E). The high degree of similarity in these trations in the micromolar range. Their expression is tightly regu- pathways strongly supports the previous reconstruction of the lated in dependence on N availability due to the energy demand of Nitrospira core metabolism for chemolithoautotrophic nitrite this transport system (54, 56). In the genome of N. lenta, the whole oxidation, which was based on only one sequenced genome (25). gene set (urtABCDE) of the urea ACB transport system is located The few genetic differences in the core pathways include addi- upstream of the urease genes (Fig. S1A and Dataset S1), suggesting tional (third) copies of respiratory complexes I and III, a second that N. lenta possesses a high-affinity uptake system for urea and, cytochrome bd oxidase, and five paralogous copies of nitrite thus, is adapted to habitats where low urea concentrations prevail. oxidoreductase (NXR) subunits NxrA and NxrB in N. mosco- In contrast, in N. moscoviensis, only urtA, which encodes the peri- viensis, whereas N. defluvii has only two paralogs of these NXR plasmic urea-binding protein UrtA, is located in close vicinity of the subunits (25) (Fig. S7 C and D). urease genes (Fig. S1A). Whether N. moscoviensis can replace the NXR, the key enzyme for nitrite oxidation, belongs to – lacking UrtBCDE proteins with the respective subunits of other the complex iron sulfur molybdoenzyme family with a ABC transporters encoded in the genome, or whether urea is taken molybdo-bis(pyranopterin guanine dinucleotide) cofactor- up by passive diffusion only, remains to be determined. containing catalytic subunit (61). The NXR of Nitrospira is lo- The accessory proteins UreD, UreE, UreF, and UreG are cated in the periplasmic space and consists of at least two + required for the formation of the Ni2 -containing metallocenter subunits (NxrA and NxrB). The third (NxrC) subunit may an- in the UreABC apoenzyme during the biosynthesis of urease chor the NXR complex in the cytoplasmic membrane and + (27). In addition, the nickel transporter UreH provides Ni2 mediate the transfer of electrons from NXR to the membrane- (27). The genome of N. moscoviensis contains the ureD, bound electron transport chain (25). The five paralogs of nxrA ureF, and ureG genes (Fig. S1A) and ureH (NITMOv2_1657). and nxrB are clustered in three genomic regions of N. moscoviensis, However, only a 180-nt-long (59 aa) gene fragment of ureE whereas five putative nxrC genes are located elsewhere in the (NITMOv2_1661) was identified, which is unlikely to encode a genome (Fig. S7C). NxrA contains the substrate-binding site functional UreE protein because homologs in other organisms with the Mo cofactor (25). Like in N. defluvii, all NxrA paralogs are approximately 200 aa in length. Although UreE is required of N. moscoviensis contain an N-terminal twin-arginine motif for a functional urease in Helicobacter (57), various other mi- for export via the twin-arginine protein translocation (Tat) croorganisms lacking ureE genes express active ureases (58). In pathway. The presence of this motif is consistent with the ureolytic microbes without UreE, this nickel-binding metal- periplasmic localization of the active site of NXR in N. moscoviensis lochaperone (59) may be substituted by chaperones of other (62) and N. defluvii (25). The periplasmic NXR is energetically nickel-dependent enzymes (58). Interestingly, in Helicobacter advantageous and likely explains the strong competitiveness under pylori two accessory proteins of nickel-dependent hydrogenase, nitrite-limited conditions of Nitrospira compared with other + HypA and HypB, are required for the incorporation of Ni2 into NOB such as Nitrobacter, whose NXR is located on the cytoplasmic urease (60). These hydrogenase maturation factors are present side of the cell membrane (25). in N. moscoviensis, which possesses an active [NiFe] hydrogenase The amino acid similarities among the NXR subunits of (23). Hence, hydrogenase chaperones might be involved in the N. moscoviensis range from 95.7 to 98.5% for NxrA, from 99.5 to assembly of urease and substitute UreE in this organism as well. 100% for NxrB, and from 18.6 to 64.1% for the putative NxrC candidates. All five NxrA copies are more similar to one of the Utilization of Organic Substrates by N. moscoviensis. Aside from two NxrA paralogs (CDS tag Nide3255) (25) in N. defluvii (87.1– formate (see Results and Discussion in the main text), we tested 87.9%) than to the other one (Nide3237) (83.6–84.2%). Inter- also whether N. moscoviensis can use other simple organic com- estingly, the similarity between the two NxrA copies in N. defluvii pounds (acetate, fumarate, succinate, citrate, and pyruvate) in is only 86.9% and, thus, lower than the similarity between all combination with nitrate as terminal electron acceptor. Acetate NxrA copies of N. moscoviensis and one NxrA (Nide3255) of could be provided by fermenting organisms in the spatial prox- N. defluvii. It is tempting to speculate that the lower similarity imity of Nitrospira in hypoxic or anoxic habitats, whereas the other between the two NxrA subunits of N. defluvii reflects a functional compounds are key metabolites that could be released by lysed differentiation, and that all NxrA of N. moscoviensis are func- cells within a biofilm. The genetic repertoire of N. moscoviensis tionally more similar to one of the NxrA paralogs (Nide3255) of includes the degradation pathways and the respiratory chain N. defluvii. Consistently, four of the five nxrA/B gene clusters in needed to use these organic compounds (Fig. S1B). Transmem- N. moscoviensis are preceded by transcriptional regulator genes, brane transporters for these substrates were not identified in the which are homologous to a regulator in N. defluvii that occurs genome, but N. moscoviensis encodes permeases of unknown directly upstream of the gene encoding NxrA Nide3255 (Fig. specificities, and we could not exclude the possibility that such S7C). The amino acid similarities between these regulators are Koch et al. www.pnas.org/cgi/content/short/1506533112 1of13 relatively high (47–73%). If the genomic localization next to include ROS detoxification by manganese or polyamines, H2O2 nxrA genes reflects a role of these regulators in the transcrip- degradation by peroxidases and thioredoxin-dependent peroxir- tional control of NXR, then the regulation of these four NXR edoxins, binding of free iron by bacterioferritin to reduce the risk paralogs in N. moscoviensis may resemble the regulation of of ROS generation, and free radical scavenging by carotenoids Nide3255 in N. defluvii. However, one of these nxr gene clusters (25). In contrast to N. defluvii, N. moscoviensis possesses a ca- in N. moscoviensis also contains a second transcriptional regu- nonical SOD and a catalase (Fig. S1B and Dataset S1). The SOD lator, which is homologous to a regulator upstream of the second of N. moscoviensis (NITMOv2_2805) binds Fe or Mn based on NxrA copy of N. defluvii (Nide3237) (Fig. S7C). Hence, in both its overall amino acid sequence similarity to other SODs that organisms, at least two different regulation mechanisms for NXR require these metal cofactors. The Fe and Mn SODs are difficult seem to be present that await confirmation and further analysis to distinguish from each other by sequence analysis, but specific in future studies. fingerprint residues (66) indicate that the enzyme of N. mosco- Each of the five NxrC candidates in N. moscoviensis has a viensis may be a tetrameric Fe SOD. N. moscoviensis possesses a homolog among the four putative NxrC subunits in N. defluvii typical monofunctional, heme-containing catalase that is encoded by (25) (Dataset S1), with two of the N. moscoviensis proteins two identical gene copies (NITMOv2_0085 and NITMOv2_4696). (NITMOv2_3617 and NITMOv2_4208) being homologous to Either catalase gene belongs to one of two identical copies of a one candidate NxrC in N. defluvii (Nide3271). All NxrC candi- 42-kbp-large Tn7 mobile element. In addition to SOD and cat- dates in both Nitrospira genomes have been identified based on alase, N. moscoviensis possesses the putative ROS defense mecha- sequence similarities to the membrane subunits of other DMSO nismsaspredictedforN. defluvii (25) except that it lacks a reductase type II family enzymes (25), but their actual functional polyamine transporter (Fig. S1B). roles and the composition of the NXR protein complex in Ni- trospira remain to be determined. SI Materials and Methods Genome Sequencing and Analysis.
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