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Diversity of Methylotrophy Pathways in the Genus Paracoccus (Alphaproteobacteria)

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Diversity of Methylotrophy Pathways in the Genus Paracoccus (Alphaproteobacteria) Diversity of Methylotrophy Pathways in the Genus Paracoccus (Alphaproteobacteria) Jakub Czarnecki1,2* and Dariusz Bartosik1 1Department of Bacterial Genetics, Institute of Microbiology, Faculty of Biology, University of Warsaw, Warsaw, Poland. 2Bacterial Genome Plasticity, Department of Genomes and Genetics, Institut Pasteur, Paris, France. *Correspondence: [email protected] htps://doi.org/10.21775/cimb.033.117 Abstract Introduction Paracoccus denitrifcans Pd 1222 is a model methy- Te genus Paracoccus (class Alphaproteobacteria, lotrophic bacterium. Its methylotrophy is based order Rhodobacterales, family Rhodobacteraceae) on autotrophic growth (enabled by the Calvin currently includes around 70 defned species and cycle) supported by energy from the oxidation of hundreds of strains whose taxonomic position has methanol or methylamine. Te growing availabil- yet to be precisely assigned (NCBI Taxonomy, ity of genome sequence data has made it possible 10 January 2018). Representatives of this genus to investigate methylotrophy in other Paracoccus have been identifed in diverse environments. Te species. Te examination of a large number of Para- original isolate and the type species, P. denitrifcans, coccus spp. genomes reveals great variability in C1 was isolated from soil (Beijerinck, 1910), like many metabolism, which have been shaped by difer- other Paracoccus spp. (Urakami et al., 1990; Siller ent evolutionary mechanisms. Surprisingly, the et al., 1996; Tsubokura et al., 1999). Numerous methylotrophy schemes of many Paracoccus strains strains have been isolated from fresh water (Sheu appear to have quite diferent genetic and bio- et al., 2018), seawater (Kim and Lee, 2015), sedi- chemical bases. Besides the expected ‘autotrophic ments (G. Zhang et al., 2016), activated sludge (Liu methylotrophs’, many strains of this genus possess et al., 2006), bioflters (Lipski et al., 1998), or from another C1 assimilatory pathway, the serine cycle, environments linked to higher organisms, such as which seems to have at least three independent plant roots (rhizosphere) (Doronina et al., 2002), origins. Analysis of the co-occurrence of diferent marine bryzoans (Pukall et al., 2003), insects (S. methylotrophic pathways indicates, on the one Zhang et al., 2016), and human tissues (opportun- hand, evolutionary linkage between the Calvin istic pathogens P. yeei and P. sanguinis) (Funke et al., cycle and the serine cycle, and, on the other hand, 2004; McGinnis et al., 2015). that genes encoding some C1 substrate-oxidizing Te ubiquity of Paracoccus spp. is due to their enzymes occur more frequently in association with great metabolic diversity and fexibility. All para- one or the other. Tis suggests that some genetic cocci have an aerobic respiratory metabolism and module combinations form more harmonious utilize multi-carbon compounds. However, many enzymatic sets, which act with greater efciency in of them can switch between diferent growth the methylotrophic process and thus undergo posi- modes, using diferent carbon and energy sources, tive selection. and employing various fnal electron acceptors. In Curr. Issues Mol. Biol. (2019) Vol. 33 caister.com/cimb 118 | Czarnecki and Bartosik the absence of oxygen, some Paracoccus spp. con- nitrate, nitrite, nitric oxide and nitrous oxide (which duct nitrate respiration (Baker et al., 1998; Kelly leads to denitrifcation – P. denitrifcans is an impor- et al., 2006). Tis process leads to denitrifcation tant model in studies on this process (Baker et al., and has been applied for the removal of nitrates 1998), thus permiting growth when oxygen is lim- from wastewater (Liu et al., 2012). In addition to ited. On the other hand, diferent electron donors ‘standard’ carbon sources, like sugars, amino acids may be used. As a consequence, P. denitrifcans has and succinate, Paracoccus strains isolated from the ability to grow chemolithoautotrophically on polluted environments can utilize xenobiotics, e.g. inorganic energy sources such as hydrogen and polycyclic aromatic hydrocarbons (PAHs), making thiosulphate (Friedrich and Mitrenga, 1981). Its them useful in bioremediation (Sun et al., 2013). autotrophic growth may also be supported by the Numerous representatives of the genus can grow oxidation of some organic C1 compounds, namely chemolithoautotrophically, coupling CO2 assimila- MeOH, MA and formate (Baker et al., 1998). Tese tion with the oxidation of inorganic compounds or compounds are oxidized to CO2, the released elec- elements, such as thiosulfate, thiocyanate, elemen- trons are used for oxidative phosphorylation, and tal sulfur, molecular hydrogen, or ferrous ions the ATP and CO2 produced are used in the Calvin (Kelly et al., 2006). Finally, many Paracoccus spp. cycle for biomass production. Tus, P. denitrifcans are methylotrophs. Most utilize methanol (MeOH) is an example of an ‘autotrophic methylotroph’, and methylamine (MA) as sole carbon and energy which lacks a ‘heterotrophic’ pathway dedicated sources, e.g. P. denitrifcans and closely related P. to the assimilation of reduced C1 units (such as the versutus and P. kondratievae (Kelly et al., 2006). serine cycle or ribulose monophosphate pathway), However, other strains isolated from environments but it can assimilate carbon from C1 compounds polluted with C1 compounds are able to metabolize afer their total oxidation (Baker et al., 1998; Chis- dimethylamine (DMA), trimethylamine (TMA), toserdova, 2011) (Fig. 6.1). N,N-dimethylformamide (DMF) (Urakami et al., Since the 1970s, numerous studies have sought 1990; Kim et al., 2001; Sanjeevkumar et al., 2013) to understand the details of C1 metabolism in or dichloromethane (Doronina et al., 1998). P. denitrifcans (Harms et al., 1985; Baker et al., Te purpose of this study is to describe the 1998), especially in strain Pd 1222, which is read- diversity of methylotrophy in the genus Paracoccus ily transformed by conjugation to enable genetic at the biochemical and genetic levels, including manipulation (Devries et al., 1989). Te results an examination of the origin and evolution of C1 of these studies have uncovered the properties of metabolism in this group of bacteria. many P. denitrifcans proteins involved in methylo- trophy (mainly MeOH and MA dehydrogenases, as well as associated proteins, i.e. those involved in the Paracoccus denitrifcans transfer of electrons from the dehydrogenases to Pd 1222 as an example of an the respiratory chain), and have shed light on the ‘autotrophic’ methylotroph regulation of their expression (Baker et al., 1998). Since its isolation at the beginning of the 20th Te whole genome sequence of P. denitrifcans century (Beijerinck, 1910), P. denitrifcans has Pd 1222 was obtained in 2006 (NCBI Genomes). been extensively studied and diferent aspects of its It has an unusual structure consisting of two energy metabolism have been revealed. Te compo- chromosomes (chromosome 1, 2.8 Mb, and chro- sition of its core respiratory chain closely resembles mosome 2, 1.7 Mb) and one large plasmid (plasmid that of the classic mitochondrial respiratory chain 1 1650 kb). Te availability of this sequence has (unlike respiratory chains of many other bacteria, permited elucidation of the genetic basis of its including E. coli), which made it a valuable model methylotrophy. P. denitrifcans Pd 1222 carries sev- for studies on the energetic processes in eukaryotes eral gene clusters responsible for C1 metabolism, (John and Whatley, 1975). However, the electron dispersed across the three replicons. Genes for the transport chain of P. denitrifcans also has many enzymes involved in the oxidation of primary C1 branches at both the entrance and exit sides of the substrates to formaldehyde are located on chromo- core. On the one hand, this allows the bacterium to some 2 (gene cluster encoding MxaFI-type MeOH utilize alternative fnal electron receptors, namely dehydrogenase and associated proteins) and Curr. Issues Mol. Biol. (2019) Vol. 33 caister.com/cimb Methylotrophy in the Genus Paracoccus | 119 Figure 6.1 Summary of the methylotrophic pathways of Paracoccus spp. P. denitrifcans Pd 1222 and P. aminovorans JCM 7685 are used as examples because these strains possess all of the methylotrophic pathways discussed in this study. The enzymes and pathways present in P. denitrifcans Pd 1222 are shown in red, those present in P. aminovorans JCM 7685 are shown in blue, and those present in both strains are shown in violet. Ddh, DMA dehydrogenase; DmfA1A2, DMFase; DmmABCD, DMA monooxygenase; FghA, S-formylglutathione hydrolase; FlhA, S-(hydroxymethyl)glutathione dehydrogenase; FolD, methylenetetrahydrofolate dehydrogenase (NADP+)/methenyltetrahydrofolate cyclohydrolase; FtfL, formate-tetrahydrofolate ligase; Gfa, S-(hydroxymethyl) glutathione synthase; MauAB, MA dehydrogenase; MxaFI, MxaFI-type MeOH dehydrogenase; PurU, formyltetrahydrofolate deformylase; Tdh, TMA dehydrogenase; Tmd, TMA N-oxide demethylase; Tmm, TMA monooxygenase; XoxF, XoxF-type MeOH dehydrogenase. *Methylated amines – TMA, DMA and MA. plasmid 1 (the mau genes encoding small and large as well as genes for fructose-1,6-bisphosphatase subunits of MA dehydrogenase and associated pro- (fp), phosphoribulokinase (prk), transketolase teins). Te second step in the methylotrophy of P. (tkt), fructose-1,6-bisphosphate aldolase (fa), denitrifcans Pd 1222 is oxidation of formaldehyde RuBisCO activating protein (cbbX), and the Calvin to formate in the glutathione-dependent pathway, cycle regulator (cbbR). which is essential for growth of this
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