Enzymatic Characterization and
            <i>In Vivo</i>
            Function of Five Terminal Oxidases in Pseudomonas aeruginosa

Arai, Hiroyuki; Kawakami, Takuro; Osamura, Tatsuya; Hirai, Toshihide; Sakai, Yoshiaki; Ishii, Masaharu

doi:10.1128/jb.02176-14

Cited by 107 publications

(152 citation statements)

References 54 publications

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“…may be able to respire oxygen, as suggested by the presence of the cbb 3 -type cytochrome c oxidase, which has a high affinity to oxygen (50,51). Therefore, Gallionellaceae sp.…”

Section: G a Ll Io N E Ll A C E A E C O M A M O N A D A C E A E R H Imentioning

confidence: 99%

“…Instead, Gallionellaceae sp. possesses the aa 3 -type cytochrome c oxidase, which typically has a low affinity to oxygen and would require high oxygen levels (51,52). This is not expected for neutrophilic FeOB, since the chemical oxidation of Fe(II) by oxygen can occur rapidly under neutral pH if oxygen is present at high concentrations.…”

Section: G a Ll Io N E Ll A C E A E C O M A M O N A D A C E A E R H Imentioning

confidence: 99%

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Metagenomic Analyses of the Autotrophic Fe(II)-Oxidizing, Nitrate-Reducing Enrichment Culture KS

Tominski

Kappler

et al. 2016

Appl Environ Microbiol

125

104

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f Nitrate-dependent ferrous iron [Fe(II)] oxidation (NDFO) is a well-recognized chemolithotrophic pathway in anoxic sediments. The neutrophilic chemolithoautotrophic enrichment culture KS originally obtained from a freshwater sediment (K. L. Straub, M. Benz, B. Schink, and F. Widdel, Appl Environ Microbiol 62:1458 -1460, 1996) has been used as a model system to study NDFO. However, the primary Fe(II) oxidizer in this culture has not been isolated, despite extensive efforts to do so. Here, we present a metagenomic analysis of this enrichment culture in order to gain insight into electron transfer pathways and the roles of different bacteria in the culture. We obtained a near-complete genome of the primary Fe(II) oxidizer, a species in the family Gallionellaceae, and draft genomes from its flanking community members. A search of the putative extracellular electron transfer pathways in these genomes led to the identification of a homolog of the MtoAB complex [a porin-multiheme cytochrome c system identified in neutrophilic microaerobic Fe(II)-oxidizing Sideroxydans lithotrophicus ES-1] in a Gallionellaceae sp., and findings of other putative genes involving cytochrome c and multicopper oxidases, such as Cyc2 and OmpB. Genome-enabled metabolic reconstruction revealed that this Gallionellaceae sp. lacks nitric oxide and nitrous oxide reductase genes and may partner with flanking populations capable of complete denitrification to avoid toxic metabolite accumulation, which may explain its resistance to growth in pure culture. This and other revealed interspecies interactions and metabolic interdependencies in nitrogen and carbon metabolisms may allow these organisms to cooperate effectively to achieve robust chemolithoautotrophic NDFO. Overall, the results significantly expand our knowledge of NDFO and suggest a range of genetic targets for further exploration.

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“…may be able to respire oxygen, as suggested by the presence of the cbb 3 -type cytochrome c oxidase, which has a high affinity to oxygen (50,51). Therefore, Gallionellaceae sp.…”

Section: G a Ll Io N E Ll A C E A E C O M A M O N A D A C E A E R H Imentioning

confidence: 99%

Section: G a Ll Io N E Ll A C E A E C O M A M O N A D A C E A E R H Imentioning

confidence: 99%

Metagenomic Analyses of the Autotrophic Fe(II)-Oxidizing, Nitrate-Reducing Enrichment Culture KS

Tominski

Kappler

et al. 2016

Appl Environ Microbiol

125

104

View full text Add to dashboard Cite

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“…The reaction mixtures were incubated for 5 min at room temperature. Oxygen consumption activity was determined amperometrically using an Apollo 4000 free radical analyzer equipped with a 2-mm ISO-OXY-2 O 2 electrode (WPI) according to the procedures described previously (10). The method for determination of the K m values for oxygen is described in SI Materials and Methods.…”

Section: Methodsmentioning

confidence: 99%

“…4C). CIO may not be fully functional under extremely low-oxygen conditions because the affinity of CIO for oxygen is low (10). We examined the inhibitory effect of cyanide on the oxygen consumption activities of the isoforms (Fig.…”

Section: Identification Of the Types Of Cbb 3 Isoforms Expressed In Tmentioning

confidence: 99%

Expression of multiplecbb₃cytochromecoxidase isoforms by combinations of multiple isosubunits inPseudomonas aeruginosa

Hirai

Osamura

Ishii

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

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The ubiquitous opportunistic human pathogen Pseudomonas aeruginosa has five terminal oxidases for aerobic respiration and uses them under different growth conditions. Two of them are cbb 3 -type cytochrome c oxidases encoded by the gene clusters ccoN1O1Q1P1 and ccoN2O2Q2P2, which are the main terminal oxidases under high-and low-oxygen conditions, respectively. P. aeruginosa also has two orphan gene clusters, ccoN3Q3 and ccoN4Q4, encoding the core catalytic CcoN isosubunits, but the roles of these genes have not been clarified. We found that 16 active cbb 3 isoforms could be produced by combinations of four CcoN, two CcoO, and two CcoP isosubunits. The CcoN3-or CcoN4-containing isoforms were produced in the WT cell membrane in response to nitrite and cyanide, respectively. The strains carrying these isoforms were more resistant to nitrite or cyanide under low-oxygen conditions. These results indicate that P. aeruginosa gains resistance to respiratory inhibitors using multiple cbb 3 isoforms with different features, which are produced through exchanges of multiple core catalytic isosubunits.

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“…In addition to contributing to the growth of P. aeruginosa under microaerobic conditions, some of these complexes have been implicated in its ability to cope with various stresses (6,12). In this issue of the Journal of Bacteriology, Arai et al conduct a comprehensive study of these complexes, probing their biochemical properties and contributions to aerobic growth (13). They describe a systematic investigation of the attributes of each enzyme, which clarified many aspects of P. aeruginosa aerobic biology and revealed a new potential role for a particular high-affinity oxidase.…”

mentioning

confidence: 99%

An Aerobic Exercise: Defining the Roles of Pseudomonas aeruginosa Terminal Oxidases

Price-Whelan

Dietrich

2014

J Bacteriol

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The opportunistic pathogen Pseudomonas aeruginosa encodes a large and diverse complement of aerobic terminal oxidases, which is thought to contribute to its ability to thrive in settings with low oxygen availability. In A lthough the Earth's atmosphere contains approximately 21% oxygen, bacteria in environments that are ostensibly aerobic still encounter zones where the concentration is much lower, due to the effects of oxygen solubility, low diffusibility, and consumption by neighboring cells. Many bacteria cope with this in part through the use of branched respiratory chains that can be modulated in response to changing conditions (1). Aerobic terminal oxidases, which catalyze electron transfer from the respiratory apparatus to oxygen, vary in their affinities and efficiencies (2). Five such enzymes have been identified in the opportunistic pathogen Pseudomonas aeruginosa (Fig. 1), and these are thought to contribute to its ability to thrive under hypoxia (1,(3)(4)(5)(6)(7)(8). A diverse collection of aerobic terminal oxidases may be especially critical for an organism that has a proficiency for persisting in biofilms, which are characterized by the formation of steep oxygen gradients (9-11). In addition to contributing to the growth of P. aeruginosa under microaerobic conditions, some of these complexes have been implicated in its ability to cope with various stresses (6,12). In this issue of the Journal of Bacteriology, Arai et al. conduct a comprehensive study of these complexes, probing their biochemical properties and contributions to aerobic growth (13). They describe a systematic investigation of the attributes of each enzyme, which clarified many aspects of P. aeruginosa aerobic biology and revealed a new potential role for a particular high-affinity oxidase.The P. aeruginosa aerobic terminal oxidases include enzymes that can use ubiquinol or cytochromes as electron donors, ones that have low or high affinities for O 2 , and a cyanide-insensitive oxidase (CIO) that functions in the presence of this endogenously produced virulence factor (12). Aside from CIO, the four other aerobic terminal oxidases encoded by the P. aeruginosa genome are the bo 3 oxidase (Cyo), the aa 3 oxidase (aa 3 ), cbb 3 oxidase 1 (cbb 3 -1), and cbb 3 oxidase 2 (cbb 3 -2). Earlier studies predicted that Cyo and aa 3 (which is most similar to the mitochondrial terminal oxidase) would have low affinities for oxygen and that CIO and the cbb 3 enzymes would have high oxygen affinities (4-6, 14, 15). In batch cultures grown under typical conditions (i.e., in nutrientrich medium and atmospheric oxygen, with vigorous shaking), the low-affinity enzymes Cyo and/or aa 3 would thus be expected to play major roles during exponential growth, when oxygen is relatively abundant. The high-affinity enzymes cbb 3 -1 and cbb 3 -2 would be expected to function primarily in stationary phase, when oxygen is relatively scarce, and/or during growth under microaerobic conditions. Hypothetically, CIO would be particularly important in stationary phase, as...

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Enzymatic Characterization and In Vivo Function of Five Terminal Oxidases in Pseudomonas aeruginosa

Cited by 107 publications

References 54 publications

Metagenomic Analyses of the Autotrophic Fe(II)-Oxidizing, Nitrate-Reducing Enrichment Culture KS

Metagenomic Analyses of the Autotrophic Fe(II)-Oxidizing, Nitrate-Reducing Enrichment Culture KS

Expression of multiplecbb₃cytochromecoxidase isoforms by combinations of multiple isosubunits inPseudomonas aeruginosa

An Aerobic Exercise: Defining the Roles of Pseudomonas aeruginosa Terminal Oxidases

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Enzymatic Characterization and In Vivo Function of Five Terminal Oxidases in Pseudomonas aeruginosa

Cited by 107 publications

References 54 publications

Metagenomic Analyses of the Autotrophic Fe(II)-Oxidizing, Nitrate-Reducing Enrichment Culture KS

Metagenomic Analyses of the Autotrophic Fe(II)-Oxidizing, Nitrate-Reducing Enrichment Culture KS

Expression of multiplecbb3cytochromecoxidase isoforms by combinations of multiple isosubunits inPseudomonas aeruginosa

An Aerobic Exercise: Defining the Roles of Pseudomonas aeruginosa Terminal Oxidases

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Expression of multiplecbb₃cytochromecoxidase isoforms by combinations of multiple isosubunits inPseudomonas aeruginosa