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. 2013 Feb 21:4:27.
doi: 10.3389/fmicb.2013.00027. eCollection 2013.

The Genome of Nitrospina gracilis Illuminates the Metabolism and Evolution of the Major Marine Nitrite Oxidizer

Sebastian Lücker  1 , Boris Nowka, Thomas Rattei, Eva Spieck, Holger Daims
Affiliations

The Genome of Nitrospina gracilis Illuminates the Metabolism and Evolution of the Major Marine Nitrite Oxidizer

Sebastian Lücker et al. Front Microbiol. .

Abstract

In marine systems, nitrate is the major reservoir of inorganic fixed nitrogen. The only known biological nitrate-forming reaction is nitrite oxidation, but despite its importance, our knowledge of the organisms catalyzing this key process in the marine N-cycle is very limited. The most frequently encountered marine NOB are related to Nitrospina gracilis, an aerobic chemolithoautotrophic bacterium isolated from ocean surface waters. To date, limited physiological and genomic data for this organism were available and its phylogenetic affiliation was uncertain. In this study, the draft genome sequence of N. gracilis strain 3/211 was obtained. Unexpectedly for an aerobic organism, N. gracilis lacks classical reactive oxygen defense mechanisms and uses the reductive tricarboxylic acid cycle for carbon fixation. These features indicate microaerophilic ancestry and are consistent with the presence of Nitrospina in marine oxygen minimum zones. Fixed carbon is stored intracellularly as glycogen, but genes for utilizing external organic carbon sources were not identified. N. gracilis also contains a full gene set for oxidative phosphorylation with oxygen as terminal electron acceptor and for reverse electron transport from nitrite to NADH. A novel variation of complex I may catalyze the required reverse electron flow to low-potential ferredoxin. Interestingly, comparative genomics indicated a strong evolutionary link between Nitrospina, the nitrite-oxidizing genus Nitrospira, and anaerobic ammonium oxidizers, apparently including the horizontal transfer of a periplasmically oriented nitrite oxidoreductase and other key genes for nitrite oxidation at an early evolutionary stage. Further, detailed phylogenetic analyses using concatenated marker genes provided evidence that Nitrospina forms a novel bacterial phylum, for which we propose the name Nitrospinae.

Keywords: Nitrospina; marine nitrogen cycle; nitrification; nitrite oxidation; nitrite oxidoreductase; nitrite-oxidizing bacteria.

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Figures

Figure 1
Figure 1
Phylogenetic affiliation of N. gracilis 3/211 (boldface). Trees were calculated using a concatenated dataset of 49 proteins (Table A1 in Appendix). Members of the phylum Planctomycetes were used as outgroup. Filled and open circles represent statistical support ≥90 and >75%, respectively. The scale bar represents 10% estimated sequence divergence. (A) Bayesian inference tree (SD = 0.009985) run for 8 M generations. In total, 6962 alignment positions were considered. (B,C) Maximum-likelihood and maximum-parsimony analysis, respectively, with 100 bootstrap iterations, using 7629 alignment positions.
Figure 2
Figure 2
Summarized results of a phylogenetic analysis of the phylome of N. gracilis 3/211. The nearest phylogenetic neighbor (closest homolog) in other sequenced genomes was determined for each protein of N. gracilis. The resulting trees were queried for the closest homolog using Phat (Frickey and Lupas, 2004). The graphs depict the phylogenetic groups displaying the largest numbers of most closely related homologs on the (A) class and (B) genus level. In total, Phat could unambiguously assign closest homologs for 2,246 proteins.
Figure 3
Figure 3
Cell metabolic cartoon based on the annotation of the N. gracilis 3/211 genome. CLD, chloride dismutase; CA, carbonic anhydrase; CysDNC, sulfate adenylyltransferase/adenylylsulfate kinase; HYD, hydrogenase; NirA, ferredoxin-nitrite reductase; NirK, Copper-containing nitrite reductase; NXR, nitrite oxidoreductase; Sir, ferredoxin-sulfite reductase; SOR, Sulfite:cytochrome c oxidoreductase. Enzyme complexes of the electron transport chain are labeled by Roman numerals. Red and orange diamonds represent cytochrome c proteins and quinones, red and blue arrows the oxidative and reductive TCA cycle, respectively.
Figure 4
Figure 4
Partial multiple sequence alignment of selected heme-copper oxidase-family members. Relationship of the enzymes is indicated by a cladogram. The oxidase type is indicated for each enzyme. Amino acid residues involved in the formation of the copper (CuB)-binding site are highlighted in color and by a symbol indicating function: dark blue, histidine residues involved in CuB-binding (c); purple, residues involved in electron transport from the high-spin heme to CuB(*), red, uncommon amino acids; orange, crosslinking tyrosine residue stabilizing one of the CuB-binding histidines (#), green and turquoise, alternative conserved residues in this position.
Figure 5
Figure 5
Phylogeny of N. gracilis 3/211 NXR (boldface) and related enzymes. Both trees show selected enzymes from the DMSO reductase type II family. Names of validated enzymes are indicated (Clr, chlorate reductase; Ddh, dimethylsulfide dehydrogenase; Ebd, ethylbenzene dehydrogenase; Nar, Nitrate reductase; Nxr, nitrite oxidoreductase; Pcr, perchlorate reductase; Ser, selenate reductase). More distantly related molybdoenzymes were used as outgroup. The scale bar represents 10% estimated sequence divergence. Pie charts indicate statistical support of nodes based on Bayesian inference, bootstrap analysis, or treepuzzle support. MB, Bayesian inference; ML, maximum-likelihood (RAxML); MP, maximum-parsimony (ProtPars); TP, maximum-likelihood (TreePuzzle). (A) Bayesian interference tree (SD = 0.006924) of the large (α) subunit. In total, 1,475 alignment positions were considered. (B) Bayesian interference tree (SD = 0.015471) of the small (β) subunit, obtained by using 532 alignment positions.
Figure 6
Figure 6
Schematic illustration of the genomic regions in N. gracilis 3/211, Ca. K. stuttgartiensis, and Ca. N. defluvii that contain genes coding for NXR, chaperones, electron carriers, cytochrome bd-like oxidases, multicopper oxidases, and conserved proteins of unknown function. Solid lines indicate proteins that are closest homologs based on protein phylogeny. Dashed lines connect homologous proteins that are not the closest relatives in the respective phylogenetic trees. Proteins and connecting lines are color-coded according to functional classes. CDS and intergenic regions are drawn to scale.
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