Reductive metabolism of the important atmospheric gas isoprene by homoacetogens.
Journal
The ISME journal
ISSN: 1751-7370
Titre abrégé: ISME J
Pays: England
ID NLM: 101301086
Informations de publication
Date de publication:
05 2019
05 2019
Historique:
received:
07
05
2018
accepted:
02
12
2018
revised:
18
10
2018
pubmed:
16
1
2019
medline:
28
10
2019
entrez:
16
1
2019
Statut:
ppublish
Résumé
Isoprene is the most abundant biogenic volatile organic compound (BVOC) in the Earth's atmosphere and plays important roles in atmospheric chemistry. Despite this, little is known about microbiological processes serving as a terrestrial sink for isoprene. While aerobic isoprene degrading bacteria have been identified, there are no known anaerobic, isoprene-metabolizing organisms. In this study an H
Identifiants
pubmed: 30643199
doi: 10.1038/s41396-018-0338-z
pii: 10.1038/s41396-018-0338-z
pmc: PMC6474224
doi:
Substances chimiques
Butadienes
0
Gases
0
Hemiterpenes
0
isoprene
0A62964IBU
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
1168-1182Références
Kesselmeier J, Staudt M. Biogenic volatile organic compounds (VOC): An overview on emission, physiology and ecology. J Atmos Chem. 1999;33:23–88.
doi: 10.1023/A:1006127516791
Atkinson R, Arey J. Gas-phase tropospheric chemistry of biogenic volatile organic compounds: A review. Atmos Environ. 2003;37:197–219.
doi: 10.1016/S1352-2310(03)00391-1
Sanadze GA. Biogenic isoprene (a review). Russ J Plant Physiol. 2004;51:729–41.
doi: 10.1023/B:RUPP.0000047821.63354.a4
Laothawornkitkul J, Taylor JE, Paul ND, Hewitt CN. Biogenic volatile organic compounds in the Earth system: Tansley review. New Phytol. 2009;183:27–51.
doi: 10.1111/j.1469-8137.2009.02859.x
Guenther A, Nicholas C, Fall R, Klinger L, Mckay WA, Scholes B, et al. A global model of natural volatile organic compound emissions. J Geophys Res. 1995;100:8873–92.
doi: 10.1029/94JD02950
Arneth A, Schurgers G, Lathiere J, Duhl T, Beerling DJ, Hewitt CN, et al. Global terrestrial isoprene emission models: Sensitivity to variability in climate and vegetation. Atmos Chem Phys. 2011;11:8037–52.
doi: 10.5194/acp-11-8037-2011
Guenther A, Karl T, Harley P, Wiedinmyer C, Palmer PI, Geron C. Estimates of global terrestrial isoprene emissions using MEGAN (model of emissions of gases and aerosols from nature). Atmos Chem Phys Discuss. 2006;6:107–73.
doi: 10.5194/acpd-6-107-2006
Guenther A, Jiang X, Heald CL, Sakulyanontvittaya T, Duhl T, Emmons LK, et al. The model of emissions of gases and aerosols from nature version 2.1 (MEGAN2.1): An extended and updated framework for modeling biogenic emissions. Geosci Model Dev. 2012;5:1471–92.
doi: 10.5194/gmd-5-1471-2012
Alvarez LA, Exton DA, Timmis KN, Suggett DJ, McGenity TJ. Characterization of marine isoprene-degrading communities. Environ Microbiol. 2009;11:3280–91.
doi: 10.1111/j.1462-2920.2009.02069.x
Kirschke S, Bousquet P, Ciais P, Saunois M, Canadell JG, Dlugokencky EJ, et al. Three decades of global methane sources and sinks. Nat Geosci. 2013;6:813–23.
doi: 10.1038/ngeo1955
Sharkey TD, Monson RK. Isoprene research - 60 years later, the biology is still enigmatic. Plant Cell Environ. 2017;40:1671–8.
doi: 10.1111/pce.12930
Sharkey TD, Wiberley AE, Donohue AR. Isoprene emission from plants: Why and how. Ann Bot. 2008;101:5–18.
doi: 10.1093/aob/mcm240
Harley PC, Monson RK, Lerdau MT. Ecological and evolutionary aspects of isoprene emission from plants. Oecologia. 1999;118:109–23.
doi: 10.1007/s004420050709
He C, Murray F, Lyons T. Monoterpene and isoprene emissions from 15 Eucalyptus species in Australia. Atmos Environ. 2000;34:645–55.
doi: 10.1016/S1352-2310(99)00219-8
Winters AJ, Adams MA, Bleby TM, Rennenberg H, Steigner D, Steinbrecher R, et al. Emissions of isoprene, monoterpene and short-chained carbonyl compounds from Eucalyptus spp. in southern Australia. Atmos Environ. 2009;43:3035–43.
doi: 10.1016/j.atmosenv.2009.03.026
Gelmont D, Stein RA, Mead JF. Isoprene- the main hydrocarbon in human breath. Biochem Biophys Res Commun. 1981;99:1456–60.
doi: 10.1016/0006-291X(81)90782-8
King J, Koc H, Unterkofler K, Mochalski P, Kupferthaler A, Teschl G, et al. Physiological modeling of isoprene dynamics in exhaled breath. J Theor Biol. 2010;267:626–37.
doi: 10.1016/j.jtbi.2010.09.028
Broadgate WJ, Malin G, Küpper FC, Thompson A, Liss PS. Isoprene and other non-methane hydrocarbons from seaweeds: A source of reactive hydrocarbons to the atmosphere. Mar Chem. 2004;88:61–73.
doi: 10.1016/j.marchem.2004.03.002
Kuzma J, Nemecek-Marshall M, Pollock WH, Fall R. Bacteria produce the volatile hydrocarbon isoprene. Curr Microbiol. 1995;30:97–103.
doi: 10.1007/BF00294190
Fall R, Copley SD. Bacterial sources and sinks of isoprene, a reactive atmospheric hydrocarbon. Environ Microbiol. 2000;2:123–30.
doi: 10.1046/j.1462-2920.2000.00095.x
Effmert U, Kalderás J, Warnke R, Piechulla B. Volatile mediated interactions between bacteria and fungi in the soil. J Chem Ecol. 2012;38:665–703.
doi: 10.1007/s10886-012-0135-5
Reeves CE, Penkett S, Bauguitte S, Law KS, Evans MJ, Bandy BJ, et al. Potential for photochemical ozone formation in the troposphere over the North Atlantic as derived from aircraft observations during ACSOE. J Geophys Res D Atmos. 2002;107:1–14.
doi: 10.1029/2002JD002415
Collins WJ, Derwent RG, Johnson CE, Stevenson DS. The oxidation of organic compounds in the troposphere and their global warming potentials. Clim Change. 2002;52:453–79.
doi: 10.1023/A:1014221225434
Pike RC, Young PJ. How plants can influence tropospheric chemistry: The role of isoprene emissions from the biosphere. Weather. 2009;64:332–6.
doi: 10.1002/wea.416
Krechmer JE, Coggon MM, Massoli P, Nguyen TB, Crounse JD, Hu W, et al. Formation of low volatility organic compounds and secondary organic aerosol from isoprene hydroxyhydroperoxide low-NO oxidation. Environ Sci Technol. 2015;10:10330–9.
doi: 10.1021/acs.est.5b02031
Zhao DF, Buchholz A, Tillmann R, Kleist E, Wu C, Rubach F. Environmental conditions regulate the impact of plants on cloud formation. Nat Commun. 2017;8:14067.
Engelhart GJ, Moore RH, Nenes A, Pandis SN. Cloud condensation nuclei activity of isoprene secondary organic aerosol. J Geophys Res. 2011;116:1–11.
doi: 10.1029/2010JD014706
Cleveland CC, Yavitt B. Consumption of atmospheric isoprene in soil. Geophys Res Lett. 1997;24:2379–82.
doi: 10.1029/97GL02451
Van Ginkel CG, De Jong E, Tilanus JWR, De Bont JAM. Microbial oxidation of isoprene, a biogenic foliage volatile and of 1,3-butadiene, an anthropogenic gas. FEMS Microbiol Lett. 1987;45:275–9.
doi: 10.1111/j.1574-6968.1987.tb02377.x
Ewers J, Freier-Schröder D, Knackmuss HJ. Selection of trichloroethylene (TCE) degrading bacteria that resist inactivation by TCE. Arch Microbiol. 1990;154:410–3.
doi: 10.1007/BF00276540
Van Hylckama Vlieg JET, De Koning W, Janssen DB. Effect of chlorinated ethene conversion on viability and activity of Methylosinus trichosporium OB3b. Appl Environ Microbiol. 1997;63:4961–4.
Van Hylckama Vlieg JE, Kingma J, Kruizinga W, Janssen DB. Purification of a glutathione S-transferase and a glutathione conjugate-specific dehydrogenase involved in isoprene metabolism in Rhodococcus sp. strain AD45. J Bacteriol. 1999;181:2094–101.
pubmed: 10094686
pmcid: 93621
Van Hylckama Vlieg JET, Leemhuis H, Jeffrey H, Spelberg L, Janssen DB. Characterization of the gene cluster involved in isoprene metabolism in Rhodococcus sp. strain AD45. J Bacteriol. 2000;187:1956–63.
doi: 10.1128/JB.182.7.1956-1963.2000
Crombie AT, El Khawand M, Rhodius VA, Fengler KA, Miller MC, Whited GM, et al. Regulation of plasmid-encoded isoprene metabolism in Rhodococcus, a representative of an important link in the global isoprene cycle. Environ Microbiol. 2015;17:3314–29.
doi: 10.1111/1462-2920.12793
El Khawand M, Crombie AT, Johnston A, Vavlline DV, McAuliffe JC, Latone JA, et al. Isolation of isoprene degrading bacteria from soils, development of isoA gene probes and identification of the active isoprene-degrading soil community using DNA-stable isotope probing. Environ Microbiol. 2016;18:2743–53.
doi: 10.1111/1462-2920.13345
Sander R. Compilation of Henry’s law constants, version 3.99. Atmos Chem Phys Discuss. 2014;14:29615–30521.
doi: 10.5194/acpd-14-29615-2014
Urakawa H, Martens-Habbena W, Stahl DA. High abundance of ammonia-oxidizing archaea in coastal waters, determined using a modified DNA extraction method. Appl Environ Microbiol. 2010;76:2129–35.
doi: 10.1128/AEM.02692-09
Engelbrektson A, Kunin V, Wrighton KC, Zvenigorodsky N, Chen F, Ochman H, et al. Experimental factors affecting PCR-based estimates of microbial species richness and evenness. ISME J. 2010;4:642–7.
doi: 10.1038/ismej.2009.153
Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, et al. Correspondence QIIME allows analysis of high- throughput community sequencing data Intensity normalization improves color calling in SOLiD sequencing. Nat Methods. 2010;7:335–6.
doi: 10.1038/nmeth.f.303
Callahan BJ, McMurdie PJ, Rosen MJ, Han AW, Johnson AJA, Holmes SP. DADA2: High-resolution sample inference from Illumina amplicon data. Nat Methods. 2016;13:581–3.
doi: 10.1038/nmeth.3869
Wang Q, Garrity GM, Tiedje JM, Cole JR. Naïve Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol. 2007;73:5261–7.
doi: 10.1128/AEM.00062-07
DeSantis TZ, Hugenholtz P, Larsen N, Rojas M, Brodie EL, Keller K, et al. Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl Environ Microbiol. 2006;72:5069–72.
doi: 10.1128/AEM.03006-05
Duhamel M, Edwards EA. Microbial composition of chlorinated ethene-degrading cultures dominated by Dehalococcoides. FEMS Microbiol Ecol. 2006;58:538–49.
doi: 10.1111/j.1574-6941.2006.00191.x
Ding C, Chow WL, He J. Isolation of Acetobacterium sp. strain AG, which reductively debrominates octa- and pentabrominated diphenyl ether technical mixtures. Appl Environ Microbiol. 2013;79:1110–7.
doi: 10.1128/AEM.02919-12
Dolfing J, Janssen DB. Estimation of Gibbs free energies of formation of chlorinated aliphatic compounds. Biodegradation. 1994;5:21–8.
Thauer RK, Jungermann K, Decker K. Energy conservation in chemotrophic anaerobic bacteria. Bacteriol Rev. 1977;41:100–80.
pubmed: 860983
pmcid: 413997
Dean JA. Lange’s handbook of chemistry. 15th ed. 2005. New York, N.Y.: McGraw-Hill; 1999. p. 577.
Ljungdahl LG, Wood HG. Total synthesis of acetate from CO2 by heterotrophic bacteria. Annu Rev Microbiol. 1969;23:515–38.
doi: 10.1146/annurev.mi.23.100169.002503
Müller V. Energy conservation in acetogenic. Appl Environ Microbiol. 2003;69:6345–53.
doi: 10.1128/AEM.69.11.6345-6353.2003
Drake HL, Küsel KMC. Acetogenic prokaryotes. The prokaryotes: Prokaryotic physiology and biochemistry. Berlin, Heidelberg: Springer; 2013. p. 1–60.
Diekert G, Wohlfarth G. Metabolism of homoacetogens. Antonie Van Leeuwenhoek. 1994;66:209–21.
doi: 10.1007/BF00871640
Bache R, Pfennig N. Selective isolation of Acetobacterium woodii on methoxylated aromatic acids and determination of growth yields. Arch Microbiol. 1981;130:255–61.
doi: 10.1007/BF00459530
Dorn M, Andreesen JR, Gottschalk G. Fumarate reductase of Clostridium formicoaceticum. Arch Microbiol. 1978;119:7–11.
doi: 10.1007/BF00407920
Seifritz C, Daniel SL, Gossner A, Drake HL. Nitrate as a preferred electron sink for the acetogen Clostridium thermoaceticum. J Bacteriol. 1993;175:8008–13.
doi: 10.1128/jb.175.24.8008-8013.1993
Terzenbach DP, Blaut M. Transformation of tetrachloroethylene to trichloroethylene by homoacetogenic bacteria. FEMS Microbiol Lett. 1994;123:213–8.
doi: 10.1111/j.1574-6968.1994.tb07224.x
Dilling S, Imkamp F, Schmidt S, Müller V. Regulation of caffeate respiration in the acetogenic bacterium Acetobacterium woodii. Appl Environ Microbiol. 2007;73:3630–36.
doi: 10.1128/AEM.02060-06
Hess V, González JM, Parthasarathy A, Buckel W, Müller V. Caffeate respiration in the acetogenic bacterium Acetobacterium woodii: A coenzyme a loop saves energy for caffeate activation. Appl Environ Microbiol. 2013;79:1942–7.
doi: 10.1128/AEM.03604-12
Hansen B, Bokranz M, Schönheit P, Kröger A. ATP formation coupled to caffeate reduction by H2 in Acetobacterium woodii NZva16. Arch Microbiol. 1988;150:447–51.
doi: 10.1007/BF00422285
Tschech A, Pfennig N. Growth yield increase linked to caffeate reduction in Acetobacterium woodii. Arch Microbiol. 1984;137:163–7.
doi: 10.1007/BF00414460
Willems A, Collins MD. Phylogenetic relationships of the genera Acetobacterium and Eubacterium sensu stricto and reclassification of Eubacterium alactolyticum as Pseudoramibacter alactolyticus gen. nov., comb. nov. Int J Syst Bacteriol. 1996;46:1083–7.
doi: 10.1099/00207713-46-4-1083
Willems A. The Family Comamonadaceae. In: Rosenberg E, DeLong EF, Lory S, Stackebrandt ETF, editors. The Prokaryotes. Berlin, Heidelberg: Springer; 2014. p. 777–851.
doi: 10.1007/978-3-642-30197-1_238
Daniel SL, Hsu T, Dean SI, Drake HL. Characterization of the H2
doi: 10.1128/jb.172.8.4464-4471.1990
Imkamp F, Müller V. Chemiosmotic energy conservation with Na
doi: 10.1128/JB.184.7.1947-1951.2002
Schuchmann K, Müller V. Autotrophy at the thermodynamic limit of life: A model for energy conservation in acetogenic bacteria. Nat Rev Microbiol. 2014;12:809–21.
doi: 10.1038/nrmicro3365
Prosen EJ, Rossini FD. Heats of formation, hydrogenation, and combustion of the monoolefin hydrocarbons through the hexenes, and of the higher 1-alkenes, in the gaseous state at 25°C. J Res Natl Bur Stand. 1946;36:269–75.
De Bruin WP, Kotterman MJJ, Posthumus MA, Schraa G, Zehnder AJB. Complete biological reductive transformation of tetrachloroethene to ethane. Appl Environ Microbiol. 1992;58:1996–2000.
pubmed: 1622277
pmcid: 195716
Koene-Cottaar FHM, Schraa G. Anaerobic reduction of ethene to ethane in an enrichment culture. FEMS Microbiol Ecol. 1998;25:251–6.
doi: 10.1111/j.1574-6941.1998.tb00477.x
Mundle SOC, Johnson T, Lacrampe-Couloume G, Perez-de-Mora A, Edwards EA, Mcmaster M, et al. Monitoring biodegradation of ethene and bioremediation of chlorinated ethenes at a contaminated site using CSIA. Environ Sci Technol. 2012;46:1731–8.
doi: 10.1021/es202792x
Elsgaard L. Reductive transformation and inhibitory effect of ethylene under methanogenic conditions in peat-soil. Soil Biol Biochem. 2013;60:19–22.
doi: 10.1016/j.soilbio.2013.01.010
Lever MA. Acetogenesis in the energy-starved deep biosphere-a paradox? Front Microbiol. 2012;2:1–18.
doi: 10.3389/fmicb.2011.00284
Avery GB, Shannon RD, White JR, Martens CS, Alperin MJ. Controls on methane production in a tidal freshwater estuary and a peatland: Methane production via acetate fermentation and CO2 reduction. Biogeochemistry. 2003;62:19–37.
doi: 10.1023/A:1021128400602
Drake HL, Daniel SL, Küsel K, Matthies C, Kuhner C, Braus-Stromeyer S. Acetogenic bacteria: what are the in situ consequences of their diverse metabolic versatilities? BioFactors. 1997;6:13–24.
doi: 10.1002/biof.5520060103
Drake HL, Gößner AS, Daniel SL. Old acetogens, new light. Ann N Y Acad Sci. 2008;1125:100–28.
doi: 10.1196/annals.1419.016
Schink B. Inhibition of methanogenesis by ethylene and other unsaturated hydrocarbons. FEMS Microbiol Lett. 1985;31:63–8.
doi: 10.1111/j.1574-6968.1985.tb01132.x
Gray CM, Helmig D, Fierer N. Bacteria and fungi associated with isoprene consumption in soil. Elem Sci Anthr. 2015;3:000053.
doi: 10.12952/journal.elementa.000053
Cleveland CC, Yavitt JB. Microbial consumption of atmospheric isoprene in a temperate forest soil microbial consumption of atmospheric isoprene in a temperate forest soil. Appl Environ Microbiol. 1998;64:172–7.
Van Hylckama Vlieg JE, Kingma J, Van den Wijngaard AJ, Janssen DB. A glutathione S-transferase with activity towards cis-1, 2-dichloroepoxyethane is involved in isoprene utilization by Rhodococcus sp. strain AD45. Appl Environ Microbiol. 1998;64:2800–5.
pubmed: 9687433
pmcid: 106775
Firn R. The main classes of NPs—Only a few pathways lead to the majority of NPs. Nature’s Chemicals. Oxford: Oxford University Press; 2009. p. 1–25.