Physiological role and redox properties of a small cytochrome c5, cytochrome c-552, from alkaliphile, Pseudomonas alcaliphila AL15-21T

Matsuno, Tomonori; Mie, Yasuhiro; Yoshimune, Kazuaki; Yumoto, Isao

doi:10.1016/j.jbiosc.2009.06.008

Cited by 5 publications

(6 citation statements)

References 30 publications

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“…( Sone and Toh, 1994 ; Bertini et al, 2006 ; Matsuno and Yumoto, 2015 ). The midpoint redox potential of cytochrome c -552 determined by redox titration (+228 mV) was almost the same as that determined by cyclic voltammetry (+224 mV) ( Matsuno et al, 2009 ). Cytochrome c -552 reacts with the terminal oxidase in the respiratory system ( Matsuno et al, 2009 ).…”

Section: Soluble Form Cytochrome C In the Gram-negsupporting

confidence: 64%

“…Gram-negative alkaliphiles have been studied far less investigated than Gram-positive alkaliphiles, probably because most of the sources for alkaliphile isolation have been terrestrial samples, such as soil. The facultative alkaliphile P. alcaliphila AL15-21 T was isolated from seawater obtained from the coast of Rumoi, Hokkaido, Japan (43°56 ′ N 141°38 ′ E) ( Yumoto et al, 2001 ), and the cytochromes c of this bacterium was studied because Gram-negative bacteria possess soluble cytochromes c ( Matsuno et al, 2007 , 2009 ; Matsuno and Yumoto, 2015 ). This property is due to the presence of periplasmic space in Gram-negative bacteria on the outer side of the membrane.…”

Section: Soluble Form Cytochrome C In the Gram-negmentioning

confidence: 99%

“…The highest amount of cytochrome c was observed in cells grown at pH 10 under low-aeration conditions. The cytochrome c content in cells grown at pH 10 under low-aeration conditions (0.47 ± 0.05 nmolmg protein -1 ) was 3.6 times higher than that in cells grown at pH 7 under high-aeration conditions, which was the lowest cytochrome c content among the tested samples (0.13 ± 0.05 nmolmg protein -1 ) ( Matsuno et al, 2009 ). The increased cytochrome c content at high pH under low-aeration conditions was similar to that observed for facultative alkaliphilic Bacillus spp.…”

Section: Soluble Form Cytochrome C In the Gram-negmentioning

confidence: 99%

“…alcaliphila AL15-21 T ( Matsuno and Yumoto, 2015 ). One particular characteristic of cytochrome c -552 is that the resting state of this protein is similar to its fully reduced state ( Matsuno et al, 2009 ). Thus, cytochrome c -552 possesses electron-retention characteristics.…”

Section: Soluble Form Cytochrome C In the Gram-negmentioning

confidence: 99%

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Formation of Proton Motive Force Under Low-Aeration Alkaline Conditions in Alkaliphilic Bacteria

et al. 2018

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In Mitchell’s chemiosmotic theory, a proton (H+) motive force across the membrane (Δp), generated by the respiratory chain, drives F1Fo-ATPase for ATP production in various organisms. The bulk-base chemiosmotic theory cannot account for ATP production in alkaliphilic bacteria. However, alkaliphiles thrive in environments with a H+ concentrations that are one-thousandth (ca. pH 10) the concentration required by neutralophiles. This situation is similar to the production of electricity by hydroelectric turbines under conditions of very limited water. Alkaliphiles manage their metabolism via various strategies involving the cell wall structure, solute transport systems and molecular mechanisms on the outer surface membrane. Our experimental results indicate that efficient ATP production in alkaliphilic Bacillus spp. is attributable to a high membrane electrical potential (ΔΨ) generated for an attractive force for H+ on the outer surface membrane. In addition, the enhanced F1Fo-ATPase driving force per H+ is derived from the high ΔΨ. However, it is difficult to explain the reasons for high ΔΨ formation based on the respiratory rate. The Donnan effect (which is observed when charged particles that are unable to pass through a semipermeable membrane create an uneven electrical charge) likely contributes to the formation of the high ΔΨ because the intracellular negative ion capacities of alkaliphiles are much higher than those of neutralophiles. There are several variations in the adaptation to alkaline environments by bacteria. However, it could be difficult to utilize high ΔΨ in the low aeration condition due to the low activity of respiration. To explain the efficient ATP production occurring in H+-less and air-limited environments in alkaliphilic bacteria, we propose a cytochrome c-associated “H+ capacitor mechanism” as an alkaline adaptation strategy. As an outer surface protein, cytochrome c-550 from Bacillus clarkii possesses an extra Asn-rich segment between the region anchored to the membrane and the main body of the cytochrome c. This structure may contribute to the formation of the proton-binding network to transfer H+ at the outer surface membrane in obligate alkaliphiles. The H+ capacitor mechanism is further enhanced under low-aeration conditions in both alkaliphilic Bacillus spp. and the Gram-negative alkaliphile Pseudomonas alcaliphila.

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Section: Soluble Form Cytochrome C In the Gram-negsupporting

confidence: 64%

Section: Soluble Form Cytochrome C In the Gram-negmentioning

confidence: 99%

Section: Soluble Form Cytochrome C In the Gram-negmentioning

confidence: 99%

Section: Soluble Form Cytochrome C In the Gram-negmentioning

confidence: 99%

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Formation of Proton Motive Force Under Low-Aeration Alkaline Conditions in Alkaliphilic Bacteria

et al. 2018

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“…The oxidation rate of cytochrome c -552 at pHs 6–10 is estimated using 100 mM buffers as follows: phosphate-NaOH buffer for pHs 6 and 7, Tris-HCl buffer for pH 8, and sodium carbonate buffer for pHs 9 and 10 [50]. Cytochrome c -552 oxidized very slowly at pHs 8–10 with the slowest at pH 8, while it oxidized rapidly at pHs 6-7.…”

Section: Redox Properties Of Cytochrome C-552mentioning

confidence: 99%

Bioenergetics and the Role of Soluble Cytochromescfor Alkaline Adaptation in Gram-Negative AlkaliphilicPseudomonas

Matsuno

Yumoto

2015

BioMed Research International

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Very few studies have been conducted on alkaline adaptation of Gram-negative alkaliphiles. The reversed difference of H+ concentration across the membrane will make energy production considerably difficult for Gram-negative as well as Gram-positive bacteria. Cells of the alkaliphilic Gram-negative bacterium Pseudomonas alcaliphila AL15-21T grown at pH 10 under low-aeration intensity have a soluble cytochrome c content that is 3.6-fold higher than that of the cells grown at pH 7 under high-aeration intensity. Cytochrome c-552 content was higher (64% in all soluble cytochromes c) than those of cytochrome c-554 and cytochrome c-551. In the cytochrome c-552-dificient mutant grown at pH 10 under low-aeration intensity showed a marked decrease in μ max⁡ [h−1] (40%) and maximum cell turbidity (25%) relative to those of the wild type. Considering the high electron-retaining abilities of the three soluble cytochromes c, the deteriorations in the growth of the cytochrome c-552-deficient mutant could be caused by the soluble cytochromes c acting as electron storages in the periplasmic space of the bacterium. These electron-retaining cytochromes c may play a role as electron and H+ condenser, which facilitate terminal oxidation at high pH under air-limited conditions, which is difficult to respire owing to less oxygen and less H+.

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Physiological function of soluble cytochrome c-552 from alkaliphilic Pseudomonas alcaliphila AL15-21T

Matsuno

Yoshimune

Yumoto

2011

J Bioenerg Biomembr

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It has been found that the alkaliphilic Gram-negative bacterium Pseudomonas alcaliphila AL15-21(T) produces a larger amount of soluble c-type cytochromes at pH 10.0 under air-limited condition than at pH 7.0 under high aeration. Cytochrome c-552 was confirmed as the major c-type cytochrome among three soluble c-type cytochromes in the strain. To understand the physiological function of cytochrome c-552, a P. alcaliphila AL15-21(T) cytochrome c-552 gene deletion mutant without a marker gene was constructed by electrotransformation adjusted in this study for the strain. The maximum specific growth rate and maximum cell turbidity of cells grown at pHs 7.0 and 10.0 under the high-aeration condition did not differ significantly between the wild-type and cytochrome c-552 deletion mutant strains. In the mutant grown at pH 10.0 under low-aeration condition, marked decreases in the maximum specific growth rate (40%) and maximum cell turbidity (25%) compared with the wild type were observed. On the other hand, the oxygen consumption rates of cell suspensions of the mutant obtained by the growth at pH 10 under low-aeration condition were slightly higher than that of the wild type. Considering the high electron-retaining ability of cytochrome c-552, the above observations could be accounted for by cytochrome c-552 acting as an electron sink in the periplasmic space. This may facilitate terminal oxidation in the respiratory system at high pH under air-limited conditions.

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Physiological role and redox properties of a small cytochrome c5, cytochrome c-552, from alkaliphile, Pseudomonas alcaliphila AL15-21T

Cited by 5 publications

References 30 publications

Formation of Proton Motive Force Under Low-Aeration Alkaline Conditions in Alkaliphilic Bacteria

Formation of Proton Motive Force Under Low-Aeration Alkaline Conditions in Alkaliphilic Bacteria

Bioenergetics and the Role of Soluble Cytochromescfor Alkaline Adaptation in Gram-Negative AlkaliphilicPseudomonas

Physiological function of soluble cytochrome c-552 from alkaliphilic Pseudomonas alcaliphila AL15-21T

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