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Anaerobic degradation of hydroaromatic compounds by newly isolated fermenting bacteria

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Abstract

Aerobic organisms degrade hydroaromatic compounds via the hydroaromatic pathway yielding protocatechuic acid which is further metabolized by oxygenase-mediated ring fission in the 3-oxoadipate pathway. No information exists on anaerobic degradation of hydroaromatics so far. We enriched and isolated from various sources of anoxic sediments several strains of rapidly growing gram-negative bacteria fermenting quinic (1,3,4,5-tetrahydroxy-cyclohexane-1-carboxylic acid) and shikimic acid (3,4,5-trihydroxy-1-cyclohexene-1-carboxylic acid) in the absence of external electron acceptors. Quinic and shikimic acid were the only ones utilized of more than 30 substrates tested. The marine isolates formed acetate, butyrate, and H2, whereas all freshwater strains formed acetate and propionate as typical fermentation products. Aromatic intermediates were not involved in this degradation. Characterization of the isolates, fermentation balances for both hydroaromatic compounds, and enzyme activities involved in one degradation pathway are presented.

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Abbreviations

BV:

benzyl viologen (1,1′-dibenzyl-4,4′-bipyridinium dichloride)

CoA:

coenzyme A

CTAB:

cetyltrimethylammonium bronide

DCPIP:

2,4-dichlorophenolindophenol

DTT:

1,4-dithiotheriol

MV:

methyl viologen (1,1′-dimethyl-4,4′-bipyridinium dichloride)

Tricine:

N-[tris-(hydroxymethyl)-methyl]-glycine

Tris:

tris-(hydroxymethyl)-aminomethane

References

  • Bartholomew (1962) Variables influencing results, and the precise definition of steps in gram staining as a means of standardizing the results obtained. Stain Technol 37: 139–165.

    Google Scholar 

  • Beri RK, Grant S, Roberts CF, Smith M, Hawkins AR (1990) Selective overexpression of the QUTE gene encoding catabolic 3-dehydroquinase in multicopy transformants of Aspergillus nidulans. Biochem J 265: 337–342

    Google Scholar 

  • Blenden DC, Goldberg HS (1965) Silver impregnation stain for Leptospira and flagella. J Bacteriol 89: 899–900

    Google Scholar 

  • Boudet A (1973) Quinic and shikimic acids in woody angiosperms. Phytochemistry 12: 363–370

    Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72: 248–254

    Google Scholar 

  • Brewster D, Jones R, Parke D (1978) The metabolism of shikimate in the rat. Biochem J 170: 257–264

    Google Scholar 

  • Bruce NC, Cain RB (1990) Hydroaromatic metabolism in Rhodococcus rhodochrous: purification and characterisation of its NAD-dependent quinate dehydrogenase. Arch Microbiol 154: 179–186.

    Google Scholar 

  • Brune A, Schink B (1990a) Pryrogallol-to-phloroglucinol conversion and other hydroxyl-transfer reactions catalyzed by cell extracts of Pelobacter acidigallici. J Bacteriol 172: 1070–1076

    Google Scholar 

  • Brune A, Schink B (1990b) A complete citric acid cycle in assimilatory metabolism of Pelobacter acidigallici, a strictly anaerobic, fermenting bacterium. Arch Microbiol 154: 394–399

    Google Scholar 

  • Brune A, Schink B (1991) Phloroglucinol pathway in the striclty anaerobic Pelobacter acidigallici: fermentation of trihydroxybenzenes to acetate via triacetic acid. Arch Microbiol (in press)

  • Buchanan BB (1969) Role of ferredoxin in the synthesis of α-ketobutyrate from propionyl coenzyme A and carbon dioxide by enzymes from photosynthetic and nonphotosynthetic bacteria. J Biol Chem 244: 4218–4223

    Google Scholar 

  • Cánovas J, Wheelis ML, Stanier RY (1968) Regulation of the enzymes of the β-ketoadipate pathway in Moraxella calcoacetica. 2. The role of protocatechuate as inducer. Eur J Biochem 3: 293–304

    Google Scholar 

  • Cashion P, Holder-Franklin MA, McCully J and Franklin M (1977) A rapid method for base ratio determination of bacterial DNA. Anal Biochem 81: 461–466

    Google Scholar 

  • Cord-Ruwisch R (1985) A quick method for the determination of dissolved and precipitated sulfides in cultures of sulfate-reducing bacteria. J Microbiol Methods 4: 33–36

    Google Scholar 

  • Diekert GB, Thauer RK (1978) Carbon monooxide oxidation by Clostridium thermoaceticum and Clostridium formicoaceticum. J Bacteriol 136: 597–606

    Google Scholar 

  • Dörner C, Schink B (1990) Clostridium homopropionicum sp. nov., a new strict anaerobe growing with 2-, 3-, or 4-hydroxybutyrate. Arch Microbiol 154: 342–348

    Google Scholar 

  • Elstner EF, Youngman RJ, Oßwald W (1985) Superoxide dismutase. In: Bergmeyer HU (ed) Methods in enzymatic analysis, 3rd edn., vol III. Verlag Chemie, Weinheim, pp 293–302

    Google Scholar 

  • Geever RF, Huiet L, Baum JA, Tyler BM, Patel VB, Rutledge BJ, Case ME, Giles NH (1989) DNA sequence, organization and regulation of the qa gene cluster of Neurospora crassa. J Mol Biol 207: 15–34

    Google Scholar 

  • Gregersen T (1978) Rapid method for distinction of gram-negative from gram-positive bacteria. Eur J Appl Microbiol Biotechnol 5: 123–127

    Google Scholar 

  • Grund E, Knorr C, Eichenlaub R (1990) Catabolism of benzoate and monohydroxylated benzoates by Amycolatopsis and Streptomyces spp. Appl Environ Microbiol 56: 1459–1464

    Google Scholar 

  • Hayaishi O, Katagiri M, Rothberg S (1957) Studies on oxygenases: pyrocatechase. J Biol Chem 229: 905–920

    Google Scholar 

  • Herbert RB (1981) The biosynthesis of secondary metabolites. Chapman & Hall, London, New York

    Google Scholar 

  • Ingledew WM, Tai CC (1972) Quinate metabolism in Pseudomonas aeruginosa. Can J Microbiol 18: 1817–1824

    Google Scholar 

  • Ingledew WM, Tresguerres MEF, Cánovas JL (1971) Regulation of the enzymes of the hydroaromatic pathway in Acinetobacter calcoaceticus. J Gen Microbiol 68: 273–282

    Google Scholar 

  • Krieg NR, Holt JG (eds) (1984) Bergey's manual of systematic bacteriology, vol 1 Williams & Wilkins, Baltiore, Md., USA

    Google Scholar 

  • Martin AK (1982) The origin of urinary aromatic compounds excreted by ruminants. 1. Metabolism of quinic acid, cyclohexanecarboxylic acid, and non-phenolic aromatic acids to benzoic acid. Br J Nutr 47: 139–154

    Google Scholar 

  • Matthies C, Mayer F, Schnk B (1989) Fermentative degradation of purescine by new strictly anaerobic bacteria. Arch Microbiol 151: 498–505

    Google Scholar 

  • Mesbah M, Premachandran U and Whitman W (1989) Precise measurement of the G+C content of deoxyribonucleic acid by high performance liquid chromatography. Int J Syst Bacteriol 39: 159–167

    Google Scholar 

  • Minamikawa T (1976) A comparative study on the metabolism of quinic acid and shikimic acid in plants. Bot Mag Tokyo 89: 141–144

    Google Scholar 

  • Möller B, Hermann K, (1983) Quinic acid esters of hydroxycinnamic acids in stone and pome fruit. Phytochemistry 22: 477–481

    Google Scholar 

  • Nishimura H; Nonaka G-I, Nishioka I (1984) Seven quinic acid gallates from Quercus stenophylla. Phytochemistry 23: 2621–2623

    Google Scholar 

  • Parke D, Ornston LN (1984) Nutritional divesity of Rhizobiaceae revealed by auxanography. J Gen Microbiol 130: 1743–1750

    Google Scholar 

  • Pfennig N, Wagener S (1986) An improved method of preparing wet mounts for photomicrographs of microogranisms. J Microbiol Methods 4: 303–306

    Google Scholar 

  • Platen H, Schink B (1987) Methanogenic degradation of acetone by an enrichment culture. Arch Microbiol 149: 136–141

    Google Scholar 

  • Platen H, Schink B (1989) Anaerobic degradation of acetone and higher ketones via carboxylation by newly isolated denitrifying bacteria. J Gen Microbiol 135: 883–891

    Google Scholar 

  • Platen H, Temmes A, Schink B (1990) Anaerobic degradation of acetone by Desulfococcus biacutus spec. nov.. Arch Microbiol 154: 355–361

    Google Scholar 

  • Procházková L (1959) Bestimmung der Nitrate im Wasser. Z Anal Chem 167: 254–260

    Google Scholar 

  • Schnell S, Brune A, Schink B (1991) Degradation of hydroxyhydroquinone by the strictly anaerobic fermenting bacterium Pelobactermassiliensis s sp. nov.. Arch Microbiol 155: 511–516

    Google Scholar 

  • Smibert AM, Krieg NR (1981) General characterization. In: Gerhardt P (ed) Manual of methods for general bacteriology. American Society for Microbiology, Washington DC, pp 409–443

    Google Scholar 

  • Stanier RY, Ingraham JL (1954) Protocatechuic acid oxidase. J Biol Chem 210: 799–808

    Google Scholar 

  • Stoeckigt J, Zenk MH (1974) Enzymic synthesis of chlorogenic acid from caffeoyl coenzyme A and quinic acid. FEBS Lett 42: 131–134

    Google Scholar 

  • Stouthamer AH (1979) The search for correlation between theoretical and experimental growth yields. In: Quayle JR (ed) Microbial biochemistry, vol 21. University Park Press, Baltimore, pp 1–47

    Google Scholar 

  • Tamoaka J and Komagate K (1984) Determination of DNA base composition by reversed-phase high-performance liquid chromatography. FEMS Microbiol Lett 25: 125–128

    Google Scholar 

  • van Kleef MAG, Duine JA (1988) Bacterial NAD(P)-independent quinate dehydrogenase is a quinoprotein. Arch Microbiol 150: 32–36

    Google Scholar 

  • Wallhöfer P, Baldwin RL (1967) Pathway of propionate fermentation in Bacteroides ruminicola. J Bacteriol 93: 504–505

    Google Scholar 

  • Wheeler LA, Halula M, DeMeo M, Sutter VL, Finegold SM (1979) Metabolism of shikimic, quinic, cyclohexanecarboxylic acids in germfree, conventional, and gnotobiotic rats. Curr Microbiol 2: 85–90

    Google Scholar 

  • Whiting GC, Coggins RA (1971) The role of quinate and shikimate in the metabolism of lactobacilli. Antonie van Leuwenhoek J Microbiol Serol 37: 33–49

    Google Scholar 

  • Whiting GC, Coggins RA (1974) A new nicotinamide-adenine dinucleotide-dependent hydroaromatic dehydrogenase of Lactobacillus plantarum and its role in formation of (-)t-3, t-4-dihydroxycycloheane-c-1-carboxylate. Biochem J 141: 35–42

    Google Scholar 

  • Widdel F, Pfenning N (1981) Studies on dissimilatory sulfate-reducing bacteria that decompose fatty acids I. Isolation of a new sulfatereducer enriched with acetate from saline environments. Description of Desulfobacter postgatei gen. nov. sp. nov. Arch Microbiol 129: 395–400

    Google Scholar 

  • Widdel F and Pfennig N (1984) Dissimilatory sulfate- or sulfurreducing bacteria. In: Krieg NR, Holt JG (eds) Bergey's manual of systematic bacteriology, vol 1, Williams & Wilkins, Baltimore, Md, pp 663–679

    Google Scholar 

  • Yoshida S, Tazaki K, Minamikawa T (1975) Occurrence of shikimic and quinic acids in angiosperms. Phytochemistry 14: 195–197

    Google Scholar 

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Author notes

  1. Andreas Brune

    Present address: Department of Microbiology and Public Health, Michigan State University, 48824-1101, East Lansing, MI, USA

  2. Berhard Schink

    Present address: Fakultät für Biologie, Universität Konstanz, Postach 5560, W-7750, Konstanz, FRG

Authors and Affiliations

  1. Lehrstuhl Mikrobiologie I, Universität Tübingen, Auf der Morgenstelle 28, W-7400, Tübingen, Germany

    Andreas Brune & Berhard Schink

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  1. Andreas Brune
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Brune, A., Schink, B. Anaerobic degradation of hydroaromatic compounds by newly isolated fermenting bacteria. Arch. Microbiol. 158, 320–327 (1992). https://doi.org/10.1007/BF00245360

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