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Genomic Analysis of the Potential for Aromatic Compounds

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Genomic Analysis of the Potential for Aromatic Compounds bs_bs_banner Environmental Microbiology (2012) 14(5), 1091–1117 doi:10.1111/j.1462-2920.2011.02613.x Minireview Genomic analysis of the potential for aromatic compounds biodegradation in Burkholderialesemi_2613 1091..1117 Danilo Pérez-Pantoja,1 Raúl Donoso,1,2 in the catabolic clusters of these pathways indicating Loreine Agulló,3 Macarena Córdova,3 recent events in its evolutionary history. In addition, a Michael Seeger,3 Dietmar H. Pieper4 and significant bias towards secondary chromosomes, Bernardo González1,2* now termed chromids, is observed in the distribution 1Center for Advanced Studies in Ecology and of catabolic genes across multipartite genomes, Biodiversity. Millennium Nucleus in Plant Functional which is consistent with a genus-specific character. Genomics. Facultad de Ciencias Biológicas, P. Strains isolated from environmental sources such as Universidad Católica de Chile. Santiago, Chile. soil, rhizosphere, sediment or sludge show a higher 2Facultad de Ingeniería y Ciencias, Universidad Adolfo content of catabolic genes in their genomes com- Ibáñez. Santiago, Chile. pared with strains isolated from human, animal or 3Laboratorio de Microbiología Molecular y Biotecnología plant hosts, but no significant difference is found Ambiental, Departamento de Química, Center for among Alcaligenaceae, Burkholderiaceae and Coma- Nanotechnology and Systems Biology, Universidad monadaceae families, indicating that habitat is more Técnica Federico Santa María, Valparaíso, Chile. of a determinant than phylogenetic origin in shaping 4Microbial Interactions and Processes Research Group, aromatic catabolic versatility. Department of Medical Microbiology, HZI – Helmholtz Centre for Infection Research. Braunschweig, Germany. Introduction Aromatic compounds are widespread in nature, being Summary found as lignin and petroleum components, xenobiotic The relevance of the b-proteobacterial Burkholderi- chemicals, aromatic amino acids and constituents of plant ales order in the degradation of a vast array of exudates, among other sources. The aerobic degradation aromatic compounds, including several priority pol- of aromatic compounds and their halogenated derivatives lutants, has been largely assumed. In this review, the by bacteria has been well studied (Pieper et al., 2010; presence and organization of genes encoding oxyge- Pérez-Pantoja et al., 2010a). The general principle of aro- nases involved in aromatics biodegradation in 80 matics degradation indicates that a broad range of periph- Burkholderiales genomes is analysed. This genomic eral reactions transforms a huge variety of compounds to analysis underscores the impressive catabolic poten- a restricted set of central intermediates, which are subject tial of this bacterial lineage, comprising nearly all of to ring-cleavage and subsequent funnelling into the Krebs the central ring-cleavage pathways reported so far in cycle. Typically, peripheral reactions consist in activation bacteria and most of the peripheral pathways of the aromatic ring through oxygenases and/or CoA involved in channelling of a broad diversity of aro- ligases generating di- or trihydroxylated intermediates matic compounds. The more widespread pathways and/or dearomatized CoA derivatives (Fig. 1) (Pérez- in Burkholderiales include protocatechuate ortho Pantoja et al., 2010a; Pieper et al., 2010). The activation ring-cleavage, catechol ortho ring-cleavage, homo- of the aromatic ring through hydroxylation (Fig. 1, outer gentisate ring-cleavage and phenylacetyl-CoA ring- circle) is commonly catalysed by members of one of three cleavage pathways found in at least 60% of genomes oxygenase families: the Rieske non-haem iron oxygena- analysed. In general, a genus-specific pattern of posi- ses which frequently catalyse the incorporation of two tional ordering of biodegradative genes is observed oxygen atoms (Gibson and Parales, 2000), the flavopro- tein monooxygenases (van Berkel et al., 2006) and the soluble diiron multicomponent oxygenases (Leahy et al., Received 20 May, 2011; accepted 11 September, 2011. *For corre- spondence. E-mail [email protected]; Tel. (+56) 2 3311619; 2003). The subsequent ring-cleavage of di- or trihydroxy- Fax (+56) 2 3311906. lated intermediates (Fig. 1, inner circle) can be catalysed © 2011 Society for Applied Microbiology and Blackwell Publishing Ltd 1092 D. Pérez-Pantoja et al. HOOC COOH OH 3-Hydroxypheny lacetic acid 4-Hydroxyphenylpyruvic acid NH2 Mha6H COOH Gallic acid COOH Phenylacetyl-CoA O COOH Anthranilic acid Benzoyl-CoA COSCoA HOOC HppDO OH COSCoA AntDO Cl HO Benzoic acid COSCoA HO OH COOH Cl OH OH HO BenDO NH OH OH 2 Paa Homogentisic acid Box 2,4-Dichlorophenol Hge Cl Gal HO Cl Sal1H HOOC 2-Aminobenzoyl-CoA COSCoA COSCoA 3,5-Dichlorocatechol Salicylic acid Cl OH O COOH OH OH OH Cca OH 2-Halobenzoic acid Cl OH Cl Cl COOH Ab Cl OH c OH COOH COOH cp4H OH Cl OhbDO T 2,4,6-Trichlorophenol O COOH Cat12 COSCoA Hxq OH HOOC IaaDO Catechol HOOC COOH NH2 6-Chlorohydroxyquinol C HOOC Cl at HO COOH Indole-3-acetic 23 COOH HO OH acid O 4-Hydroxyphenylacetic acid BphDO CHO O COOH N COOH H CHO Hpc HO COOH COOH COOH OH OH OH Homoprotocatechuic Cca COOH Cl acid HO Central Salicylic OH Biphenyl COOH COOH COOH O COOH acid OH Me t abolism HOOC COOH Cl Cl OH 3-Chlorocatechol H C OH COOH 3 CH3 Gen Tmo O Mhb6H COOH zDO COOH HO OH Cb Benzene Phenol HO O COOH CHO Gentisic acid 3-Hydroxybenzoic acid Dhc HOOC OHC COOH HOOC COOH Cl OH HOOC Chlorobenzene HO HOOC Isophthalic COOH HOOC OH DO acid mt COOH COOH C H C CH NH 2 CHO 3 3 COOH COOH 2,3-Dihydroxy-p-cumic acid HOOC OH HOOC NH2 NH 2 HO Protocatechuic O O COOH COOH COOH acid COOH P Phthalic acid h CHO b OH COOH 2-Aminophenol OH 3H COOH H3C CH 3 COOH p -Cumic acid Dhp COOH Hxq HO OH COOH HO HO OH HO OH Hydroquinone HOOC O CH OH H2N COOH 3 Vanillic COOH 3-Hydroxyanthranilic OH OH O CH3 Hydroxyquinol OH acid Isovanillic Terephthalic acid 2,3-Dihydroxyphenylpropionic 4-Hydroxybenzoic acid acid acid acid Res4H DapDO PcmH O HO H C OH Mhp2H HO 3 OH OH p-Cresol HOOC 2,4’-Dihydroxyacetophenone OH Resorcinol 3-Hydroxyphenylpropionic acid Fig. 1. Overview of peripheral and ring-cleavage pathways for bacterial catabolism of aromatic compounds. The inner circle includes the structures of dearomatized and ring-cleavage products. The outer circle includes the structures of aryl-CoA and dihydroxylated ring-cleavage intermediates. Dotted lines indicate multiple steps. Gene markers listed in Table 1 are bolded. by either intradiol or extradiol dioxygenases. While all bacterial lineage whose genomic sequences have been intradiol dioxygenases described thus far belong to the completed (Chain et al., 2006; Gross et al., 2008; Mattes same superfamily, members of at least three different et al., 2008; Pérez-Pantoja et al., 2008). Based on the families are reported to be involved in the extradiol ring- available literature in the biodegradation field, the excep- cleavage of hydroxylated aromatics. Altogether, the inven- tional catabolic potential of Burkholderiales revealed tory of oxygenases involved in activation and cleavage by genomic analysis is not surprising because of the of the aromatic ring is extensive and phylogenetically large number of strains belonging to this order that diverse, including several different families that have have been isolated by its biodegradative abilities (a been recently compiled for phylogenomic studies (Pérez- non-comprehensive list restricted to genus Burkholderia Pantoja et al., 2010b). Analysis of the distribution of these is found in Denef, 2007). The relevance of Burkholderiales aromatic oxygenases-encoding genes among available for environmental biotechnology has been largely pro- bacterial genome sequences has shown that members of posed based on these culture-dependent methods the Burkholderiales order of the b-proteobacteria harbour (O’Sullivan and Mahenthiralingam, 2005; Chiarini et al., the most impressive potential for aromatic compounds 2006; Denef, 2007). However, the unequivocal confirma- catabolism. These biodegradative abilities become out- tion of Burkholderiales preponderance in bioremediation standing in highly specialized degraders belonging to this processes occurring in multiple environmental systems © 2011 Society for Applied Microbiology and Blackwell Publishing Ltd, Environmental Microbiology, 14, 1091–1117 Degradation of aromatic compounds in Burkholderiales 1093 has been raised with the emergence of stable isotope families in these 80 sequenced genomes is not homo- probing techniques that links functional activity to specific geneous since 48 strains belong to the Burkholderiaceae members of microbial communities (Madsen, 2006). family. The other strains are distributed among the Using this in situ approach, a key biodegradative role for Comamonadaceae (16), Alcaligenaceae (8) and Oxalo- Burkholderiales has been reported in bioremediation of bacteraceae (5) families (Fig. 2). Three unclassified multiple aromatic compounds including: polychloroby- Burkholderiales species, Thiomonas intermedia K12, phenyls (Tillmann et al., 2005; Uhlik et al., 2009), toluene Methylibium petroleiphilum PM1 and Leptothrix cholodnii (Sun et al., 2010), benzene (Liou et al., 2008; Xie et al., SP-6 were also analysed. 2011), benzoate (Pumphrey and Madsen, 2008), salicy- The genome database for Burkholderiales includes late (Singleton et al., 2005), phenol (Manefield et al., bacteria that can be classified, somewhat artificially, 2005), pentachlorophenol (Mahmood et al., 2005), 2,4- based on their source of isolation: (i) human host,
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