MICROBIOLOGIcAL REVIEWS, June, 1993, p. 451-509 Vol. 57, No. 2 0146-0749/93/020451-59$02.00/0 Copyright X) 1993, American Society for Microbiology Biology, Ecology, and Biotechnological Applications of Anaerobic Bacteria Adapted to Environmental Stresses in Temperature, pH, Salinity, or Substrates SUSAN E. LOWE,lt* MAHENDRA K. JAIN,2 AND J. GREGORY ZEIKUS1'2'3 Department ofBiochemistry' and Department ofMicrobiology and Public Health,3 Michigan State University, East Lansing, Michigan 48824, and Michigan Biotechnology Institute, Lansing, Michigan 489092 INTRODUCTION ........................................................................... 453 THERMOPHILES .......................................................................... 454 Ecology, Diversity, and Taxonomy........................................................................... 454 Physiology, Biochemistry, and Genetics ........................................................................... 461 Downloaded from Overview.......................................................................... 461 Catabolism and autotrophy of methanogens and acetogens.......................................................461 (i) Methanogenesis and autotrophy........................................................................... 461 (ii) Acetogenesis and autotrophy of C. thermoaceticum .........................................................462 (iii) Novel properties of sulfur/sulfate/thiosulfate reducers and other species..............................462 Ethanolic fermentation of saccharides........................................................................... 462 (i) Comparison of carbon and electron flow in Thermoanaerobacter brockii and Clostridium thermoceflum........................................................................... 462 (ii) Properties of alcohol dehydrogenases from thermoanaerobes ............................................463 http://mmbr.asm.org/ (iii) Novel properties of other ethanol-producing species .......................................................463 Biopolymer degradation mechanisms........................................................................... 464 (i) Celiulolytic system of C. thermocewum ..........................................................................464 (ii) Amylolytic systems of thermoanaerobes........................................................................464 (iii) Xylanolytic systems of thermoanaerobes ......................................................................465 Adaptation Mechanisms........................................................................... 466 Overview........................................................................... 466 Thermostable enzymes ........................................................................... 466 (i) General features.......................................................................... 466 (ii) Unique catalytic activities........................................................................... 467 on July 25, 2018 by guest Membranes and other cell components ........................................................................... 468 Comparison with aerobic thermophiles ........................................................................... 468 Biotechnological Features........................................................................... 468 Overview.......................................................................... 468 Alcohol and organic-acid fermentations........................................................................... 469 Thermophilic enzymes and genes.......................................................................... 470 Anaerobic waste treatment.......................................................................... 470 DEHALOGENATING AND CARBON MONOXIDE-UTIUZING ORGANISMS ...............................471 Ecology, Diversity, and Taxonomy........................................................................... 471 Overview........................................................................... 471 CO-utilizing bacteria........................................................................... 472 Anaerobes that perform dehalogenations .......................................................................... 473 (i) PCE degradation........................................................................... 473 (ii) Dichloroethane and trichloroethane degradation.............................................................474 (iii) Tetrachloromethane and tetrachloroethene degradation ..................................................474 (iv) PCP degradation ........................................................................... 474 Physiology and Biochemistry ...............474 CO fermentation.474 Carbon monoxide dehydrogenase.474 Dehalogenation.....................................475 (i) PCE dechlorination by D. tiedjei.475 (ii) PCE dechlorination by Methanosarcina spp.475 (iii) CCl4 dechlorination...475 (iv) Metabolism of tetrachloromethane.475 * Corresponding author. t Present address: Bristol-Myers Squibb Pharmaceutical Re- search Institute, 5 Research Parkway, P.O. Box 5100, Wallingford, CTs 06492-7660. 451 452 LOWE ET AL. MICROBIOL. REV. Adaptation Mechanisms................................................476 Overview........................476 Substrate versatility.476 Comparison with aerobic dehalogenators and CO utilizers.476 (i) CO-utilizing microorganisms.476 (ii) Dehalogenation by microorganisms.476 Biotechnological Features.476 CO utilization.476 Biodegradation of halogenated compounds.476 SYNTROPHS........................477 Ecology, Diversity, and Taxonomy....477 Overview........................477 Acid-utilizing bacteria................... 477 (i) Acetate utilizers.477 (ii) Propionate utilizers.478 (iii) Butyrate utilizers.478 Downloaded from (iv) Long-chain fatty acid utilizers.........................478 (v) Benzoate and 3-chlorobenzoic acid utilizers.479 Sulfate-reducing bacteria.479 Physiology and Biochemistry.479 Inhibition of growth of syntrophs.479 (i) Inhibition by H2 or formate.479 (ii) Inhibition by VFAs.479 (iii) Inhibition by acetate.479 Nutrient influence on syntrophs.480 http://mmbr.asm.org/ Tricultures of syntrophs.480 Fatty acid-degrading pathways..............................80 (i) Butyrate degradation.480 (ii) Propionate degradation.480 Adaptation Mechanisms.481 Biotechnological Features.483 Overview......... ........483 Syntrophic biomethanation granules.483 ACIDOPHILES AND ALKALIPHILES.483 and Diversity.483 Ecology on July 25, 2018 by guest Overview.................................................483 Gastrointestinal ecosystems.484 Carbohydrate fermentation.485 Protein fermentation....485 Sedimentary ecosystems.486 Thermophilic ecosystems.487 Physiology and Metabolism.487 Overview........................487 Acidophilic fermentations.487 (i) Acetone and butanol fermentation.487 (ii) Ethanol fermentation.487 (iii) Lactate, propionate, and succinate fermentations.488 Alkaliphilic fermentations.488 Adaptation Mechanisms .....489 Overview...................o489 Internal pH and maintenance of PMF.489 Membrane and cellular components.489 Comparison with aerobic acidophiles and alkaliphiles.490 Biotechnological Features.491 Overview........................491 Higher-value organic acids.491 Acetone-butanol-ethanol fermentation.491 Fermented foods ................... 492 HALOPHILES.492 Ecology, Diversity, and Taxonomy.492 Overview........................492 Ecology and diversity.492 Taxonomy.493 Physiology and Metabolism.493 Growth features.493 Metabolic types............................................ 494 VOL. 57, 1993 ANAEROBIC BACTERIA ADAPTED TO ENVIRONMENTAL STRESS 453 Adaptation Mechanisms............................................... AftA Internal salt concentration .....................................................494 Enzymes..................... ................ ~~~~~~~~~~~~0.................................................494 Membranes and other cell components ........................ Biotechnological Features............................................. Higher-value organic acids ...................! Coal gasification and waste treatment.......................... .495 CONCLUSIONS AND FUTURE RESEARCH DIRECTIONS. .495 Aft, ACKNOWLEDGMENTS ....... ................... ooo ... ...... AUtu INTRODUCTION tions. By extreme conditions we mean those which are far from the normal conditions used to describe the origins of To address the mechanisms used by specialized groups of physiological biochemistry (i.e., pH, neutral; temperature, chemoorganotrophic anaerobes that exist under extreme 37°C; atmosphere, aerobic; salinity, 1.5%; substrate, glu- environments, it is pertinent to outline the evolution of the cose). These normal growth conditions were used to under- Downloaded from Earth and the sequence of events which led to the biosphere stand the foundations of how normal cells (i.e., animal cells, and the kinds of bacteria we have today. It is generally Escherichia coli, and Bacillus subtilis) function. In recent agreed that life arose when the Earth was cooling and years we have learned that prokaryotic microorganisms can occupied by numerous volcanic features. The early atmo- differ from eukaryotic cells in part because they have sphere was reducing and free of oxygen and contained H2, adapted to grow under extreme growth conditions of tem- CH4, CO, NH3, HCN, and H2S. One line of evolutionary perature (>1000C), salinity (saturated NaCl),