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The Genome Of Nitrospina Gracilis Illuminates The Metabolism And Evolution Of The Major Marine Nitrite Oxidizer

S. Lücker, Boris Nowka, T. Rattei, E. Spieck, H. Daims
Published 2013 · Biology, Medicine

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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.
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10.1111/1462-2920.12801
The hidden seasonality of the rare biosphere in coastal marine bacterioplankton.
L. Alonso-Sáez (2015)
10.1038/ismej.2013.144
Metagenomic analysis of size-fractionated picoplankton in a marine oxygen minimum zone
Sangita Ganesh (2014)
10.1575/1912/8450
Productivity, metabolism and physiology of free-living Chemoautotrophic Epsilonproteobacteria
Jesse C. McNichol (2016)
Syddansk Universitet Metagenomic binning recovers a transcriptionally active Gammaproteobacterium linking methanotrophy to partial denitrification in an anoxic oxygen minimum zone
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10.3389/fmars.2017.00213
Diversity and Transcriptional Levels of RuBisCO Form II of Sulfur-Oxidizing γ-Proteobacteria in Coastal-Upwelling Waters with Seasonal Anoxia
Bárbara Léniz (2017)
10.1111/1758-2229.12837
Autotrophic carbon fixation pathways along the redox gradient in oxygen‐depleted oceanic waters
P. Ruiz-Fernández (2020)
10.1039/c9em00296k
Plant rhizosphere, soil microenvironment, and functional genes in the nitrogen removal process of bioretention.
T. Chen (2019)
10.1007/s00248-016-0897-3
Detection and Diversity of the Nitrite Oxidoreductase Alpha Subunit (nxrA) Gene of Nitrospina in Marine Sediments
Sundas Rani (2016)
10.1016/j.marpolbul.2017.10.039
Perturbation of seafloor bacterial community structure by drilling waste discharge.
T. T. Nguyen (2018)
10.1093/GBE/EVV239
Genome Analysis of Structure-Function Relationships in Respiratory Complex I, an Ancient Bioenergetic Enzyme.
M. D. Esposti (2016)
Expanding the knowledge on nitrifying bacteria and their ecological niches
Katharina Kitzinger (2015)
10.1038/s41396-019-0443-7
Uncultured Nitrospina-like species are major nitrite oxidizing bacteria in oxygen minimum zones
X. Sun (2019)
10.1111/1462-2920.15265
The bacterial sulfur cycle in expanding dysoxic and euxinic marine waters.
Daan M van Vliet (2020)
10.1073/pnas.1605501113
Hydrogen peroxide detoxification is a key mechanism for growth of ammonia-oxidizing archaea
J. Kim (2016)
10.3389/fmicb.2019.00115
Editorial: The Responses of Marine Microorganisms, Communities and Ecofunctions to Environmental Gradients
H. Dang (2019)
10.1007/s00284-020-02193-y
Spatio-Temporal Variations in the Abundance and Community Structure of Nitrospira in a Tropical Bay.
Tie-Qiang Mao (2020)
10.1007/s00709-019-01442-7
Multidomain ribosomal protein trees and the planctobacterial origin of neomura (eukaryotes, archaebacteria)
T. Cavalier-Smith (2020)
10.1101/2020.03.05.977850
Exploring the upper pH limits of nitrite oxidation: diversity, ecophysiology, and adaptive traits of haloalkalitolerant Nitrospira
Anne Daebeler (2020)
10.1021/cr400518y
How biology handles nitrite.
L. Maia (2014)
10.1038/ismej.2016.56
Genomics of a phototrophic nitrite oxidizer: insights into the evolution of photosynthesis and nitrification
J. Hemp (2016)
10.3389/fmicb.2018.01249
Sediment Microbial Communities Influenced by Cool Hydrothermal Fluid Migration
L. Zinke (2018)
10.1101/648329
Widespread microbial mercury methylation genes in the global ocean
Emilie Villar (2019)
10.1126/science.aar6329
Stealth reactions driving carbon fixation
S. Ragsdale (2018)
10.1038/ismej.2017.25
Integrated metabolism in sponge–microbe symbiosis revealed by genome-centered metatranscriptomics
L. Moitinho-Silva (2017)
10.1016/j.biotechadv.2016.04.003
Insights into microbial diversity in wastewater treatment systems: How far have we come?
I. Ferrera (2016)
10.1101/2020.06.09.141952
Genomic and kinetic analysis of novel Nitrospinae enriched by cell sorting
Anna J Mueller (2020)
10.1111/1462-2920.12300
NxrB encoding the beta subunit of nitrite oxidoreductase as functional and phylogenetic marker for nitrite-oxidizing Nitrospira.
M. Pester (2014)
10.1002/bit.25880
Assessment of nitric oxide (NO) redox reactions contribution to nitrous oxide (N2O) formation during nitrification using a multispecies metabolic network model
O. Perez-Garcia (2016)
10.1101/317552
Unexpected versatility in the metabolism and ecophysiology of globally relevant nitrite-oxidizing Nitrotoga bacteria
Andrew M Boddicker (2018)
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