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Microbial respiratory quinones as indicator of ecophysiological redox conditions

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Abstract

The bacterial respiratory quinones and membrane phospholipid fatty acids (PLFA) were measured to test the biochemical responses to the redox conditions after the respiration of diverse electron acceptors by microorganisms. Shewanella putrefaciens strain CN32 was examined for its growth with O2, nitrate, ferrihydrite, ferric citrate, and sulfite as electron acceptors. The same parameters were also measured for Desulfovibrio desulfuricans strain G-20, Geobacter metallireducens strain GS-15, Thioploca spp., two strains of magnetotactic bacteria (Magneteospirilum magnetotactium marine vibrioid strain MV-1 and M. sp. strain AMB-1), and environmental sediments. Microorganisms with aerobic respiratory of oxygen (MV-1 and AMB-1) have high ratios of monounsaturated to saturated straight chain PLFA and ubiquinone to menaquinone ratios; while those that conduct strict anaerobic respirations (G-20 with sulfate and GS-15 with ferric iron) have low ratios of monounsaturated to saturated straight chain PLFA and uniquinone to menaquinone ratios. The facultative respiratory of nitrate (Thioploca) has these parameters in the middle. The ratios of menaquinones to ubiquinones in CN32 cells systematically increase according to the increase of redox potential and bioavalibility of electron acceptors. The correlation between σUQ-n/σMK-n ratios and redox conditions indicates the structure of respiratory quinone responses sensitively to the microbial ecophysiological conditions.

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References

  • Baird H H, Nivens D E, Parker J H, White D C (1985). The biomass, community structure, and spatial distribution of the sedimentary microbiota from a high-energy area of the deep sea. Deep-Sea Res, 32 (9): 1089–1099

    Article  Google Scholar 

  • Bazylinski D A, Frankel R B (2004). Magnetosome formation in prokaryotes. Nat Rev Microbiol, 2 (3): 217–230

    Article  Google Scholar 

  • Bazylinski D A, Frankel R B, Jannasch H W (1988). Anaerobic magnetite production by a marine magnetotactic bacterium. Nature, 334 (6182): 518–519

    Article  Google Scholar 

  • Beliaev A S, Klingeman D M, Klappenbach J A, Wu L, Romine M F, Tiedje J M, Nealson K H, Fredrickson J K, Zhou J (2005). Global transcriptome analysis of Shewanella oneidensis MR-1 exposed to different terminal electron acceptors. J Bacteriol, 187 (20): 7138–7145

    Article  Google Scholar 

  • Bligh E G, Dyer W J (1959). A rapid method of total lipid extraction and purification. Can J Biochem Physiol, 97: 911–917

    Google Scholar 

  • Collins M D, Jones D (1981). Distribution of isoprenoid quinone structural types in bacteria and their taxonomic implication. Microbiol Rev, 45 (2): 316–354

    Google Scholar 

  • Fossing H, Gallardo V A, Jørgensen B B, Hüttel M, Nielsen L P, Schulz H, Canfield D E, Forster S, Glud R N, Gundersen J K, Küver J, Ramsing N B, Teske A, Thamdrup B, Ulloa O (1995). Concentration and transport of nitrate by the mat-forming sulfur bacterium Thioploca. Nature, 374 (6524): 713–715

    Article  Google Scholar 

  • Frolova G M, Pavel’ K G, Shparteeva A A, Nedashkovskaia O I, Gorshkova N M, Ivanova E P, Mikha.lov V V (2005). Lipid composition of novel Shewanella species isolated from far Eastern seas. Mikrobiologiia, 74 (6): 766–771

    Google Scholar 

  • Gennis R B, Stewart V (1996) Respiration in Escherichia coli and Salmonella typhimurium: cellular and molecular biology. 2nd edition. Neidhardt F C, eds. Washington D C: American Society for Microbiology, 217–261

    Google Scholar 

  • Geyer R, Peacock A D, White D C, Lytle C, Van Berkel G J (2004). Atmospheric pressure chemical ionization and atmospheric pressure photoionization for simultaneous mass spectrometric analysis of microbial respiratory ubiquinones and menaquinones. J Mass Spectrom, 39 (8): 922–929

    Article  Google Scholar 

  • Guckert J B, Antworth C P, Nichols P D, White D C (1985). Phospholipid, ester-linked fatty acid profiles as reproducible assays for changes in prokaryotic community structure of estuarine sediments. FEMS Microbiol Letters, 31: 147–158

    Google Scholar 

  • Hedrick D B, White D C (1986). Microbial respiratory quinones in the environment: a sensitive liquid chromatographic method. J Microbiol Methods, 5 (5–6): 243–254

    Article  Google Scholar 

  • Hiraishi A (1999). Isoprenoid quinones as biomarkers of microbial populations in the environment. J Biosci Bioeng, 88 (5): 449–460

    Article  Google Scholar 

  • Hiraishi A, Ueda Y, Ishihara J (1998). Quinone profiling of bacterial communities in natural and synthetic sewage activated sludge for enhanced phosphate removal. Appl Environ Microbiol, 64(3): 992–998

    Google Scholar 

  • Holländer R (1976). Correlation of the function of demethylmenaquinone in bacterial electron transport with its redox potential. FEBS Lett, 72 (1): 98–100

    Article  Google Scholar 

  • Hunter K S, Wang Y, van Cappellen P (1998). Kinetic modeling of microbially-driven redox chemistry of subsurface environments: coupling transport, microbial metabolism and geochemistry. J Hydrol (Amst), 209 (1–4): 53–80

    Article  Google Scholar 

  • Jørgensen B B, Gallardo V A (1999). Thioploca spp: filamenteous sulfur bacteria with nitrate vacuoles. FEMS Microbiol Ecol, 28 (4): 301–313

    Google Scholar 

  • Li Y L, Peacock A, White D C, Geyer R, Zhang C L (2007). Spatial patterns of bacterial signature biomarkers in marine sediments of the Gulf of Mexico. Chem Geol, 238 (3–4): 168–179

    Article  Google Scholar 

  • Li Y L, Vali H, Yang J, Phelps T J, Zhang C L (2006). Reduction of iron oxides enhanced by a sulfate-reducing bacterium and biogenic H2S production. Geomicrobiol J, 23 (2): 103–117

    Article  Google Scholar 

  • Lovley D R, Coates J D, Blunt-Harris E L, Phillips E J P, Woodward J C (1996). Humic substances as electron acceptors for microbial respiration. Nature, 382(6590): 445–448

    Article  Google Scholar 

  • Lovley D R, Giovannoni S J, White D C, Champine J E, Phillips E J P, Gorby Y A, Goodwin S (1993). Geobacter metallireducens gen. nov. sp. nov., a microorganism capable of coupling the complete oxidation of organic compounds to the reduction of iron and other metals. Arch Microbiol, 159(4): 336–344

    Article  Google Scholar 

  • Ludvigsen L, Albrechtsen H-J, Ringelberg D B, Ekelund F, Christensen T H (1999). Distribution and composition of microbial populations in a landfill leachate contaminated aquifer. Microbial Ecology, 37 (3): 197–207

    Article  Google Scholar 

  • Matsunaga T, Sakaguchi T, Tadokoro F (1991). Magnetite formation by a magnetic bacterium capable of growing aerobically. Appl Microbiol Biotechnol, 35 (5): 651–655

    Article  Google Scholar 

  • McCaffrey M A, Farrington J W, Repeta D J (1989). Goechemical implications of the lipid composition of Thioploca spp. From the Peru upwelling region 15°S. Org Geochem, 14 (1): 61–68

    Article  Google Scholar 

  • McHatton S C, Barry J P, Jannasch H W, Nelson D C (1996). High nitrate concentrations in vacuolate, autotrophic marine Beggiatoa spp. Appl Environ Microbiol, 62 (3): 954–958

    Google Scholar 

  • Moser D P, Nealson K H (1996). Growth of the facultative anaerobe Shewanella putrefaciens by elemental sulfur reduction. Appl Environ Microbiol, 62 (6): 2100–2105

    Google Scholar 

  • Myers C R, Myers J M (2004). Shewanella oneidensis MR-1 restores menaquinone synthesis to a menaquinone-negative mutant. Appl Environ Microbiol, 70 (9): 5415–5425

    Article  Google Scholar 

  • Myers C R, Nealson K H (1988). Bacterial manganese reduction and growth with manganese oxide as the sole electron acceptor. Science, 240 (4857): 1319–1321

    Article  Google Scholar 

  • Nealson K H, Little B (1997). Breathing manganese and iron: solid-state respiration. Adv Appl Microbiol, 45: 213–239

    Article  Google Scholar 

  • Nealson K H, Moser D P, Saffarini D A (1995). Anaerobic electron acceptor chemotaxis in Shewanella putrefaciens. Appl Environ Microbiol, 61 (4): 1551–1554

    Google Scholar 

  • Nealson K H, Myers C R (1992). Microbial reduction of manganese and iron: new approaches to carbon cycling. Appl Environ Microbiol, 58 (2): 439–443

    Google Scholar 

  • Nealson K H, Saffarini D (1994). Iron and manganese in anaerobic respiration: environmental significance, physiology, and regulation. Annu Rev Microbiol, 48 (1): 311–343

    Article  Google Scholar 

  • Nealson K H, Scott J (2006). Ecophysiology of the Genus Shewanella. The Prokaryotes, 6: 1133–1151

    Article  Google Scholar 

  • Otte S, Kuenen J G, Nielsen L P, Paerl H W, Zopfi J, Schulz H N, Teske A, Strotmann B, Gallardo VA, Jørgensen BB (1999). Nitrogen, carbon, and sulfur metabolism in natural Thioploca samples. Appl Environ Microbiol, 65 (7): 3148–3157

    Google Scholar 

  • Parkes R J, Taylor J (1983). The relationship between fatty acid distributions and bacterial respiratory types in contemporary marine sediments. Estuar Coast Shelf Sci, 16 (2): 173–174

    Article  Google Scholar 

  • Parkes R J (1987). Analysis of microbial communities within sediments using biomarkers. 141–177. In: Fletcher M, Gray T R Gand Jones J, eds. Ecology of Microbial Communities. Cambridge University Press: Cambridge

    Google Scholar 

  • Perry KA, Kostka J E, Luther G W, Nealson K H (1993). Mediation of sulfur speciation by a Black Sea facultative anaerobe. Science, 259 (5096): 801–803

    Article  Google Scholar 

  • Polglase W J, Pun W T, Withaar J (1966). Lipoquinones of Escherichia coli. Biochim Biophys Acta, 118 (2): 425–426

    Google Scholar 

  • Ringelberg D B, Sutton S, White D C (1997). Biomass, bioactivity and biodiversity: microbial ecology of the deep subsurface: analysis of ester-linked phospholipid fatty acids. FEMS Microbiol Rev, 20 (3–4): 371–377

    Article  Google Scholar 

  • Ruebush S S, Icopini G A, Brantley S L, Tien M (2006). In vitro enzymatic reduction kinetics of mineral oxides by membrane fractions from Shewanella oneidensis MR-1. Geochim et Cosmochim Acta, 70 (1): 56–70

    Article  Google Scholar 

  • Schröder I, Johnson E, de Vries S (2003). Microbial ferric iron reductases. FEMS Microbiol Rev, 27 (2–3): 427–447

    Article  Google Scholar 

  • Schulz H N, Jørgensen B B (2001). Big bacteria. Annu Rev Microbiol, 55 (1): 105–137

    Article  Google Scholar 

  • Søballe B, Poole R K (1999). Microbial ubiquinones: multiple roles in respiration, gene regulation and oxidative stress management. Microbiology, 145 (8): 1817–1830

    Article  Google Scholar 

  • Straub K L, Benz M, Schink B (2001). Iron metabolism in anoxic environments at near neutral pH. FEMS Microbiol Ecol, 34 (3): 181–186

    Article  Google Scholar 

  • Whistance G R, Threlfall D R (1968). Effect of anaerobiosis on the concentrations of demethylmenaquinone, menaquinone and ubiquinone in Escherichia freundii, Proteus mirabilis and Aeromonas punctata. Biochem J, 108 (3): 505–507

    Google Scholar 

  • Wissenbach U, Ternes D, Unden G (1992). An Escherichia coli mutant containing only demethylmenaquinone, but no menaquinone: effects on fumarate, dimethylsulfoxide, trimethylamine N-oxide and nitrate respiration. Arch Microbiol, 158 (1): 68–73

    Article  Google Scholar 

  • White D C, Davis W M, Nickels J S, King J D, Bobbie R J (1979). Determination of the sedimentary microbial biomass by extractible lipid phosphate. Oecologia, 40 (1): 51–62

    Article  Google Scholar 

  • White D C, Ringelberg D B, MacNaughton S J, Alugupalli S A, Schram D (1997) Signature lipid biomarker analysis for quantitative assessment in situ of environmental microbial ecology. In: Molecular markers in environmental geochemistry. Eganhouse R P, ed. ACS Symposium Series 671, American Chemical Society, Washington DC, 22–34

    Chapter  Google Scholar 

  • Zhang C L, Huang Z Y, Cantu J, Pancost R D, Brigmon R L, Lyons TW, Sassen R (2005). Lipid biomarkers and carbon isotope signatures of a microbial (Beggiatoa) mat associated with gas hydrates in the gulf of Mexico. Appl Environ Microbiol, 71 (4): 2106–2112

    Article  Google Scholar 

  • Zopfi J, Kjaer T, Nielsen L P, Jørgensen B B (2001). Ecology of Thioploca spp.: nitrate and sulfur storage in relation to chemical microgradients and influence of Thioploca spp. on the sedimentary nitrogen cycle. Appl Environ Microbiol, 67 (12): 5530–5537

    Article  Google Scholar 

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Li, Y. Microbial respiratory quinones as indicator of ecophysiological redox conditions. Front. Earth Sci. China 4, 195–204 (2010). https://doi.org/10.1007/s11707-010-0019-3

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