Abstract
Erythrobacteraceae is one of the two families that belong to the order Sphingomonadales, and it is affiliated with the class Alphaproteobacteria. The family Erythrobacteraceae includes five genera – Altererythrobacter, Croceicoccus, Erythrobacter, Erythromicrobium and Porphyrobacter – for a total of 33 species, including 29 with validly published names and 4 new species. Members of the family are Gram-negative, aerobic, rod-shaped or pleomorphic coccoid bacteria; they are motile or nonmotile, chemo-organotrophic, produce pigments (yellow, orange, red or pink), and do not form spores. Some species require biotin. Most members contain bacteriochlorophyll a (BChl a), several types of carotenoids, and monosaccharide-type glycosphingolipid. Representatives of the clade have been isolated from diverse environments: wild rice, cold-seep sediment, desert sand, tepid water, seawater, tidal flats, marine sediment, and marine invertebrates. Whole-genome sequencing has been reported in only two genera of the Erythrobacteraceae family, including Erythrobacter (three strains) and Porphyrobacter (one strain). Family members offer a valuable source of information for further studies focused on aerobic anoxygenic phototrophic (AAP) metabolism, physiological nature, and high potential for biotechnological purposes by the presence of important hydrolases.
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Taxonomy: Historical and Current
Erythrobacteraceae (E.ry.thro.bac.te.ra’ceae. N.L. masc. n. Erythrobacter type genus of the family; -aceae ending to denote a family; N.L. fem. pl. n. Erythrobacteraceae the Erythrobacter family) (Lee et al. 2005 emend. Xu et al. 2009).
Erythrobacteraceae DNA mol% G+C content varies between 54.5 and 71.5. The type genus is Erythrobacter. Erythrobacteraceae is phylogenetically closest related to the family Sphingomonadaceae. These two families integrate the order Sphingomonadales, and they are affiliated with the class Alphaproteobacteria.
Physiologically, the group is very similar. Members are Gram-negative, rod-shaped, or pleomorphic coccoid bacteria and aerobic chemoorganotrophs. Most species contain carotenoids and require NaCl for growth (although it is not essential in many cases), some species contain BChl a. Autotrophic growth has not been reported, but one genus may be facultative photoheterotrophs. Members of this taxon have been isolated mainly from aquatic environments, but there are also isolation reports from sediment, sand, and rice.
Erythrobacter, the type genus of the Erythrobacteraceae family, was originally described by Shiba and Simidu in 1982. Members of this genus are orange- and pink-pigmented Gram-negative bacteria. They are aerobic chemoorganotrophs that are motile by subpolar flagella. Erythrobacter are halophilic carotenoids that are able to use glucose, pyruvate, acetate, butyrate, and glutamate as sole organic carbon sources, but not methanol. Strains require biotin and are able to hydrolyze gelatin, tween 80, and alginate. Although these organisms do not grow phototrophically, the presence of bacteriochlorophyll a indicates that this taxon is most closely related to the Rhodospirillaceae family (Rhodospirillales order), so it was maintained as a new genus inside this family. Later, the nonphotosynthetic Sphingomonas group was included in the α-4 subclass of Proteobacteria (Yabuuchi et al. 1990), as well as the Erythrobacter-Porphyrobacter-Erythromicrobium cluster, which was defined to be most closely related to members of the genus Sphingomonas (Yurkov et al. 1994). A new order was proposed to accommodate this clade. The Sphingomonadales order was created based on 16S rRNA sequence comparisons, as well as phenotypic and morphological characteristics (Yabuuchi and Kosako 2005).
Strain representatives of the Porphyrobacter genus proposed by Fuerst et al. (1993) shared ultrastructural similarities with members of the Planctomycetales. However, 16S rRNA sequence data indicated that these bacteria shared a position within the Alfa subclass of the Proteobacteria with Erythrobacter longus, but they were distinguishable in their sequences and in other characteristics, such as their requirement of vitamins for growth; acetate, glutamate, and butyrate utilization; gelatin hydrolysis; and quantitative differences in detectable cellular fatty acids.
The photosynthetic apparatus, biochemical, morphological, and 16S rRNA sequence data for strain E5T (= DSM 8510T) also supported the proposal that a new genus and a new species should be described. The Erythromicrobium genus was introduced by Yurkov et al. (1992) as a genus of freshwater, obligatory aerobic, facultative, photoheterotrophic bacteria that included five species tentatively identified on the basis of DNA–DNA hybridization and phenotypic data (Yurkov et al. 1991): Erythromicrobium sibiricum, Erythromicrobium ursincola, Erythromicrobium ezovicum, Erythromicrobium hydrolyticum, and Erythromicrobium ramosum. However, the genus was validly published in 1994 with Erythromicrobium ramosum as the type strain (Yurkov et al. 1994) and the unique valid named species in the genus. In 1997, the genus Erythromicrobium was taxonomically reorganized, resulting in the exclusion of E. sibiricum and E. ursincola from the genus, being transferred to new genera, Sandaracinobacter and Erythromonas, respectively (Yurkov et al. 1997). Subsequently, phylogenetic analysis of the class Alphaproteobacteria based on 16S rRNA sequence comparisons through phylogenetic tree led to the reclassification of the genera Erythrobacter (Shiba and Simidu 1982), Porphyrobacter (Fuerst et al. 1993), and Erythromicrobium (Yurkov et al. 1994) into a new family named Erythrobacteraceae by Lee and colleagues (2005).
Further, the Altererythrobacter genus was suggested by Kwon et al. (2007) to accommodate new species in the clade. Altererythrobacter showed high similarity to the genus Erythrobacter but did not share its phyletic line. Another taxonomic rearrangement was related to reclassification of Erythrobacter luteolus (Yoon et al. 2005a) as Altererythrobacter luteolus comb. nov. (Kwon et al. 2007).
The last genus introduced in Erythrobacteraceae family was Croceicoccus (Xu et al. 2009), represented by aerobic and chemoheterotrophic bacteria containing carotenoids but not BChl a. The emended description of the family Erythrobacteraceae was also included in the study of Xu et al. (2009).
At the time of writing (September 2012), the family Erythrobacteraceae consisted of five genera (Table 9.1 ) with 33 species (Tables 9.2 , 9.3 , 9.4 , and 9.5 ): Erythrobacter (type genus) (13 species, 2 of which were only effectively published), Altererythrobacter (12 species, 2 of which were only effectively published) Croceicoccus (1 species), Erythromicrobium (1 species), and Porphyrobacter (6 species).
Phylogenetic Structure of the Family and Its Genera
The phylogenetic reconstruction of the 33 type species of the family Erythrobacteraceae based on 16S rRNA gene sequence is represented in Fig. 9.1 . Erythrobacteraceae is most closely related to Sphingomonadaceae. These families belong to the order Sphingomonadales, and it is affiliated with the class Alphaproteobacteria.
The five genera (Erythrobacter, Altererythrobacter, Croceicoccus, Erythromicrobium and Porphyrobacter) currently recognized within the Erythrobacteraceae family are separated in the tree based on the topology created using the randomized axelerated maximum likelihood algorithm (RAxML; Stamatakis 2006). Representative sequences from Rhodospirillaceae and Rodobiaceae, which are closely related taxa, were used as outgroups. In addition, a 10 % maximum frequency filter was applied in order to remove hypervariable positions and potentially misplaced bases from the alignment of the sequences. The scale bar in Fig. 9.1 represents 0.02-bp substitutions per nucleotide position.
Molecular Analyses
DNA–DNA Hybridization
DNA-DNA hybridization (DDH) studies have been performed on several Erythrobacteraceae family members including Altererythrobacter, Erythrobacter, and Porphyrobacter genera, confirming the taxonomic positions of the species proposed in each taxon. Tables 9.6 , 9.7 , and 9.8 summarize the DNA–DNA similarities among the type strains of the Erythrobacteraceae family.
Levels of DNA–DNA relatedness between A. marensis MSW-14T and its closest relatives, A. epoxidivorans KCCM 42314T and A. luteolus KCTC 12311T were determined to be 26.0–27.3 % and 9.8–15.2 %, respectively (Seo and Lee 2010). The value between A. xinjiangensis S3-63T and the type strain of the phylogenetically most closely related species A. marinus H32T was 54.5 ± 2 % (Xue et al. 2012). DNA–DNA similarity between A. troitsensis KMM 6042T and A. dongtanensis was 34.4 % ± 7.6 % (Nedashkovskaya et al. 2013).
DNA–DNA relatedness between E. citreus strains RE35F/1T and RE10F/45 was (79 % ± 6 %). However, values between E. citreus strains and E. litoralis DSM 8509T were 25 % ± 2 % and 34 % ± 2 %, respectively, and between E. citreus and Erythromicrobium ramosum DSM 8510T were 20 % ± 3 % and 34 % ± 4 %, respectively (Denner et al. 2002). E. flavus strains SW-46T and SW-52 exhibited DNA–DNA relatedness levels of 94.0 % and 94.7 % against each other, although E. flavus strains and the type strains of E. longus DSM 6997T, E. litoralis DSM 8509T, and E. citreus DSM 14432T were 4.2 % and 3.6 %; 6.0 % and 7.4 %; and 13.1 % and 14.7 %, respectively (Yoon et al. 2003).
Levels of DNA relatedness observed between E. aquimaris strains SW-110T, SW-116, and SW-140 were 88.5–102.1 %, but DNA relatedness of E. aquimaris strains against E. longus, E. litoralis, E. citreus, and E. flavus were between 5.3 % and 12.7 % (Yoon et al. 2004a). DNA similarity between E. seohaensis SW-135T and E. gaetbuli SW-161T was 12.3 %. Moreover, E. seohaensis SW-135T and E. gaetbuli SW-161T exhibited DNA similarity levels of 9.7–20.2 % and 8.5–18.9 % against E. longus, E. litoralis, E. citreus, E. flavus, and E. aquimaris (Yoon et al. 2005b).
DNA–DNA hybridization similarity among four E. vulgaris strains (i.e., 022-2-10T, 022-2-9, 022-2-12 and 022-4-7) was 94–98 %. DNA relatedness between E. vulgaris and E. flavus KCCM 41642T, E. citreus DSM 14432T, E. litoralis DSM 8509T, E. aquimaris KCCM 41818T, and E. longus ATCC 33941T were 39 %, 37 %, 33 %, 33 %, and 30 %, respectively (Ivanova et al. 2006). DNA–DNA relatedness values between E. nanhaisediminis T30T and E. aquimaris JCM 12189T, E. seohaensis JCM 21815T, E. citreus JCM 21816T, E. vulgaris DSM 17792T, and E. longus JCM 6170T were 56.9 %, 40.3 %, 19.7 %, 14.7 %, and 14.5 %, respectively (Xu et al. 2010). DNA–DNA relatedness between E. pelagi UST081027-248T and E. citreus DSM14432T, E. seohaensis DSM 16221T, E. flavus DSM16421T, E. vulgaris DSM 17792T, and E. nanhaisediminis DSM 16125T were 62 %, 48 %, 24 %, 14 %, and 14 %, respectively (Wu et al. 2012).
P. sanguineus strains IAM 12620T and ATCC 25661 showed DNA–DNA relatedness of 88 % against each other. In addition, the DNA relatedness between P. sanguineus IAM 12620T and its phylogenetic neighbors Erytromicrobium ramosum DSM 8510T, P. tepidarius DSM 10594T, P. neustonensis DSM9434T, Erytrobacter litoralis DSM8509T, Erytrobacter longus IFO 14126T, Blastomonas natatoria DSM 3183T, and Sphingomonas paucimobilis IFO 13935T were 38 %, 36 %, 31 %, 18 %, 14 %, 2 %, and <1 %, respectively (Hiraishi et al. 2002). DNA–DNA relatedness between P. neustonensis DSM 9434T and P. tepidarius DSM 10594T, P. sanguineus ATCC 25661 and IAM 12620T, Erytromicrobium ramosum DSM 8510T, Erytrobacter litoralis DSM8509T, Erytrobacter longus IFO 14126T, Blastomonas natatoria DSM 3183T, and Sphingomonas paucimobilis IFO 13935T were 38 %, 32 %, 29 %, 29 %, 14 %, 11 %, 4 %, and <1 %, respectively (Hiraishi et al. 2002).
DNA–DNA relatedness of P. cryptus ALC-2T and ALC-3 strains against P. neustonensis, P. tepidarius, Erythrobacter longus, and Erythromicrobium ramosum were 25 %, 31 %, 35 %, 40 %, 19 %, 20 %, 22 %, and 21 %, respectively. DDH relatedness of P. neustonensis against P. tepidarius, E. longus, and E. ramosum were 24 %, 21 %, and 24 %, respectively. Values for P. tepidarius against E. longus and E. ramosum were 22 % and 24 %, respectively. DNA similarity between E. longus and E. ramosum was 25 % (Rainey et al. 2003). P. donghaensis strains SW-132T and SW-158 exhibited a mean level of DNA–DNA relatedness of approximately 86 %. Values between P. donghaensis strains and the type strains of Porphyrobacter species (i.e., P. neustonensis, P. tepidarius, P. sanguineus and P. cryptus) were in the range of 9.4–20.3 % (Yoon et al. 2004b). Levels of DNA–DNA relatedness between P. dokdonensis DSW-74T and the type strains P. neustonensis, P. tepidarius, P. sanguineus, P. cryptus, and P. donghaensis were in the range of 9–25 % (Yoon et al. 2006).
Genome Analysis
As of May 2013, no type strains genome sequence is available in the Erythrobacteraceae family. However, three genomes belonging to the Erythrobacter genus have been reported, but only one is completely closed. Moreover, a draft genome has also stated for the Porphyrobacter genus. The main features of these genomes are summarized in Table 9.9 .
The E. litoralis genome, strain HTCC2594, was isolated from a depth of 10 m in the Sargasso Sea, Atlantic Ocean, and cultured in a low-nutrient heterotrophic medium. It contains one circular chromosome of 3,052,398 bp, 3.011 protein coding genes, one copy of 16S-23S-5S rRNA, 45 tRNA genes encoding 19 aminoacyl-tRNA sequences, and 63.07 % G+C content (Oh et al. 2009). No plasmids are present. Moreover, the HTCC2594 genome lacks reaction center genes for phototrophic metabolism, genes for CO2 fixation such as ribulose-1,5-bisphosphate carboxylase/oxygenase, and components of the reverse trichloroacetic acid cycle. The HTCC2594 strain encodes three distinct epoxide hydrolases with enantioselectivity towards styrene oxides, which may be exploited for biotechnological purposes (Woo et al. 2007; Oh et al. 2009).
So far, two other Erythrobacter draft genomes have been documented: Erythrobacter sp. strain NAP1, available as 2 scaffolds, and Erythrobacter sp. strain SD-21, available as 19 scaffolds. The NAP1 strain, which is an aerobic, anoxygenic, phototrophic bacterium, was isolated by plating on minimal medium from a water sample collected in the Northwest Atlantic in 2000 (Kolber et al. 2001; Koblízek et al. 2003). The genome of Erythrobacter sp. NAP1 consists of a single circular chromosome of 3,264,238 bp with 3.177 putative genes that cover 92 % of the genome, one copy of each of the rRNA genes, 45 genes for tRNAs, G+C content of 61 %, and a complete set of genes for bacteriochlorophyll biosynthesis and reaction center proteins (Koblízek et al. 2011). The continuous 38.9-kb-long photosynthetic gene cluster is organized as follows: bchIDO-crtCDF-bchCXYZ-pufBALM-tspO-bchPORF-bchG-ppsR-ppaA-bchFNBHLM-lhaA-puhABC-acsF-puhEhemA-cycA. Homologs of regulatory genes ppaA (cobalamin binding) and ppsR (crtJ homologue) are also present in the gene cluster, but most of the carotenoid biosynthesis genes are located outside the cluster (Koblízek et al. 2011). The NAP1 genome contains a full set of genes for heme biosynthesis; γ-aminolevulinic acid is synthesized through the Shemin (C4) pathway, besides a complete set of genes for the siroheme biosynthesis pathway, although final enzymes of cobalamin (vitamin B12) biosynthesis are missing.
Although the NAP1 strain lacks the genes of any autotrophic CO2 fixation pathway (Koblízek et al. 2011), this strain may augment heterotrophic growth with light harvesting encoded by the puf operon and ribulose-1,5-bisphosphate carboxylase/oxygenase independent CO2 fixation (Koblízek et al. 2003). Genes for nitrogenase or nitrate reductase are also absent in this genome, which is consistent with its inability to grow on nitrate. The NAP1 genome offers a valuable source of information for further studies focused on AAP metabolism and physiological nature (Koblízek et al. 2011).
Erythrobacter sp. strain SD-21 was isolated from surface sediment from the San Diego Bay, based on its ability to oxidize soluble Mn(II) to insoluble Mn(III, IV) oxides. The genome of SD-21 strain contains 2,970,874 bp, 2.941 protein coding genes that cover 85 % of the genome, one copy of the rRNA genes, 41 genes for tRNAs, and 62.9 % G+C content (http://www.ncbi.nlm.nih.gov/genome/browse/; https://moore.jcvi.org/moore/) (Table 9.9 ). The SD-21 strain was reported as the first bacterium within the alpha-4 Proteobacteria that is able to oxidize Mn(II) as well as the first marine Gram-negative bacterium containing Mn(II)-oxidizing proteins (Francis et al. 2001). In addition to being a robust Mn(II) oxidizer, SD-21 clusters with the aerobic anoxygenic phototrophs, which may comprise as much as 11 % of the microbial community in the upper ocean and exert a significant impact on global carbon cycling (Kolber et al. 2001). This nonphotosynthetic, manganese(II)-oxidizing bacterium (Francis et al. 2001; Oh et al. 2009) has a new type of manganese-oxidizing enzyme (Anderson et al. 2009) and may serve as a useful model for studying the mechanism of Mn(II) oxidation within the α-Proteobacteria and the biological function of bacterial Mn(II) oxidation.
Porphyrobacter sp. strain AAP82 was isolated from the Huguangyan Maar Lake in southern China. The genome of the AAP82 strain has a BioProject number in the Genebank database (http://www.ncbi.nlm.nih.gov/genome/browse/), but no valid publication has been reported yet. This AAP bacterium represents an important microbial component in the upper layers of the water column in various freshwater lakes. The AAP82 strain genome is available in 52 scaffolds and contains 2,899,072 bp, 2789 coding sequences, one copy of each of the rRNA genes, 44 genes for tRNAs, and G+C content of 67.3 % (RAST server; Aziz et al. 2008).
The comparative analyses among these four genomes of the Erythrobacteraceae family has been represented by Genome Atlas (Fig. 9.2 ) based on the GeneWiz browser 0.94 server. Sphingomonas wittichii RW1 was used as the reference genome.
Phages
Two prophage sequences are reported in the genome of Erythrobacter litoralis strain HTCC2594: a large prophage region (157,555–185,998 bp) and a medium prophage region (2,812,472–2,826,784 bp) (Oh et al. 2009). Based on the Rast Server annotation (Aziz et al. 2008), which uses the subsystem feature counts, three sequences have been allocated in the phages: a prophages category from Erythrobacter sp. NAP1 and two from Erythrobacter sp. SD-21 genomes. The main functions of the proteins in this category were phage packaging machinery and phage capsid proteins. The comparative chromosomal region for the phage genes among the three Eryhtrobacter strains is represented in Fig. 9.3 . No sequence has been reported for Porphyrobacter sp. strain AAP82 in phages, prophages, transposable elements, or plasmids categories.
Phenotypic Analyses
Family Erythrobacteraceae Lee, Liu, Anzai, Kim, Aono and Oyaizu (2005). Emend Xu, Wu, Wang, Wang, Oren and Wu (2009)
Erythrobacteraceae (E.ry.thro.bac.te.ra’ceae. N.L. masc. n. Erythrobacter type genus of the family; -aceae ending to denote a family; N.L. fem. pl. n. Erythrobacteraceae the Erythrobacter family.
The main features of Erythrobacteraceae family members are summarized below and listed in Tables 9.1 , 9.2 , 9.3 , 9.4 , and 9.5 . The family Erythrobacteraceae was circumscribed on the basis of the phylogenetic analysis of 16S rRNA gene sequences, hybridizations based on similarities between DNA–DNA (DDH), and phenotypic characteristics. The family is phenotypically, metabolically, and ecologically similar. It basically includes aerobic chemoorganotrophs, but one genus may be facultative photoheterotrophs.
Type genus: Erythrobacter.
Genus Erythrobacter Shiba and Simidu (1982)
Erythrobacter (Gr. adj. eiythrus red; M. L. masc. n. bacter rod or staff; M. L. mas. n. Erythrobacter red rod)
Cells are yellow, orange, orange-yellow, or red-orange; ovoid to rod-shaped; and 0.3–3.0 by 0.5–5.0 um. The cells contain ubiquinone-10 (Q-10) as the predominant respiratory lipoquinone. Optimal growth occurs at temperatures between 25 °C and 37 °C and at pH values between 7.0 and 8.0. They are Gram-negative, non-spore-forming, and multiply by binary fission. Cells are motile by means of polar or subpolar flagella, or they are nonmotile. Most species contain carotenoids, require NaCl for growth, utilize glucose but do not hydrolyze starch or gelatin, and do not reduce nitrate. The Voges-Proskauer test is mostly negative. They are aerobic chemoorganotrophs; only two species present bacteriochlorophyll a. No growth is reported anaerobically in the light and no autotrophic growth occurs with H2. Although small amounts of acid are produced from a wide range of carbohydrates under microaerobic conditions, metabolism is predominantly respiratory. Most species are mainly susceptible to chloramphenicol. Methanol is not utilized. Oxidase and catalase can be produced. The G+C of the DNA is 58.9–67 mol%.
Type species: Erythrobacter longus.
The genus currently contains 13 species, although only 2 of which were effectively published: E. longus (Shiba and Simidu 1982); E. litoralis (Yurkov et al. 1994); E. citreus (Denner et al. 2002); E. flavus (Yoon et al. 2003); E. aquimaris (Yoon et al. 2004a); E. gaetbuli and E. seohaensis (Yoon et al. 2005b); E. vulgaris (Ivanova et al. 2006); E. gangjinensis (Lee et al. 2010); E. nanhaisediminis (Xu et al. 2010); E. pelagi (Wu et al. 2012); “E. jejuensis” (Yoon et al. 2013); and “E. marinus” (Jung et al. 2012). Erythrobacter luteolus was isolated from a tidal flat of the Yellow Sea in Korea (Yoon et al. 2005a) has been transferred to Altererythrobacter luteolus comb. nov. (Kwon et al. 2007). Tables 9.1 and 9.2 summarize the properties of the Erythrobacter genus.
Genus Altererythrobacter Kwon, Woo, Yang, Kang, Kang, Kim, Sato and Kato (2007). Emend Xue, Zhang, Cai, Dai, Wang, Rahman, Peng and Fang (2012)
Altererythrobacter (Al.ter.e.ryth’ro.bac’ter. L. adj. alius, alterius another, other, different; N.L. masc. n. Erythrobacter a genus name; N.L. masc. n. Altererythrobacter another or different Erythrobacter, because the genus shows high similarity to the genus Erythrobacter but does not share its phyletic line).
Cells are Gram-negative and motile or nonmotile; the color of cell suspensions and colonies can be yellow, orange-red, or ochre. Strains produce catalase and can be positive or negative for oxidase. Methanol-soluble pigments are species-dependent and are characterized by absorption maxima at 447 and 473 nm. They do not contain BChl a as a photosynthetic pigment. The major polar lipids are phosphatidylethanolamine, phosphatidylglycerol, diphosphatidylglycerol, and sphingoglycolipid. Anaerobic growth does not occur on marine agar (MA) or on MA supplemented with nitrate. The dominant fatty acid is C18:1 ω7c. They do not produce H2S or indole, do not utilize manose, and do not hydrolyze gelatin. The dominant respiratory quinone is Q10. The optimal growth temperature occurs in mesophilic conditions. All species can grow in the presence of NaCl, although it is not essential in many cases. The DNA G+C content is 54.5–67.2 mol%.
Type species: Altererythrobacter epoxidivorans.
The genus currently contains 12 species, although only 2 of which were effectively published: A. luteolus (Yoon et al. 2005a; Kwon et al. 2007); A. epoxidivorans (Kwon et al. 2007); A. indicus (Kumar et al. 2008); A. marinus (Lai et al. 2009); A. marensis (Seo and Lee 2010); A. aestuarii (Park et al. 2011); A. dongtanensis (Fan et al. 2011); A. ishigakiensis (Matsumoto et al. 2011); A. namhicola (Park et al. 2011); A. xinjiangensis (Xue et al. 2012); “A. gangjinensis” (Jeong et al. 2013); “A. troitsensis” (Nedashkovskaya et al. 2013).
Tables 9.1 and 9.3 summarize the properties of Altererythrobacter.
Genus Croceicoccus Xu, Wu, Wang, Wang, Oren and Wu (2009)
Croceicoccus [Cro.ce.i.coc’cus. L. adj. croceus yellow, golden; N.L. masc. n. coccus (from Gr. masc. n. kokkos) grain or berry; N.L. masc. n. Croceicoccus referring to a yellow coccoid-shaped bacterium].
Cells are Gram-negative and non-spore-forming cocci. Cells are motile and occur in pairs. Young cultures show pleomorphic coccoid cells (0.8–1.0 mm). Colonies on complex agar containing peptone, casamino acids, and yeast extract are 1–2 mm in diameter, circular, smooth, elevated, opaque, and yellow pigmented. They are oxidase negative, catalase positive, divide by binary division, and are capable of producing multifibrillar stalk-like fascicle structures on the cell surface. Cells are aerobic and chemoheterotrophic. They contain carotenoids but not BChl a. No growth occurs anaerobically in the light.
Ubiquinone-10 is the major respiratory quinone. The polar lipid profiles comprise phosphatidylglycerol, two unidentified glycolipids, phosphatidylcholine, and an unidentified phospholipid. The major fatty acids are anteiso-C15: 0, iso-C14 : 0 and iso-C15 : 0. Cells are susceptible to ampicillin (10 mg), bacitracin (0.04 U), cefalexin (30 mg), ceftriaxone (30 mg), chloramphenicol (30 mg), erythromycin (15 mg), gentamicin (10 mg),minocycline (30 mg), neomycin (30 mg), novobiocin (30 mg), penicillin (10 mg), streptomycin (10 mg), and tetracycline (30 mg). The phylogenetic position is in the α-4 subgroup of the class Alphaproteobacteria. The G+C of the DNA of the type strain of the single species is 71.5 mol%.
Type species: Croceicoccus marinus.
Tables 9.1 and 9.4 summarizes the properties of Croceicoccus marinus and Erythromicrobium ramosum.
Genus Erythromicrobium Yurkov, Stackebrandt, Holmes, Fuerst, Hugenholtz, Golecki, Gad'on, Gorlenko, Kompantseva and Drews (1994)
Erythromicrobium (E.ry.thro.mi.cro’bi.um. Gr. adj. erythrus, red; Gr. adj. micros, small; Gr. n. bios, life; N.L. n. Erythromicrobium, red microbe).
The description of Erythromicrobium is supported by biochemical, morphological, and 16S rDNA sequence data. Cells are Gram-negative, rod-shaped cells, 0.6–1.0 by 1.3–2.5 μm, and usually motile by means of flagella. Branching may occur. The cells are orange and contain BChl a and carotenoids. The major carotenoids are the very polar compound erythroxanthin sulfate and bacteriorubixanthinal. Optimal growth occurs at temperatures between 25 °C and 30 °C and at pH values between 7.0 and 8.5. Multiplication occurs by binary or ternary fission. Cells are aerobic chemoorganotrophs and facultative photoheterotrophs. No growth occurs anaerobically in the light. Ribulose diphosphate carboxylase is not detected. No fermentation or denitrification activities occur. Methanol is not utilized. Cells are phylogenetically related to members of the Proteobacteria α-4 subclass. They are frequently found in freshwater habitats and are not halophilic. The G+C of the DNA of the type strain of the single species is 64.2 mol%.
Type species: Erythromicrobium ramosum.
Erythromicrobium ramosum is the only valid species published in this genus (Yurkov et al. 1994). “Erythromicrobium sibiricum,” “Erythromicrobium ursincola”, “Erythromicrobium ezovicum,” and “Erythromicrobium hydrolyticum” were tentatively allocated in this genus by Yurkov et al. (1991). However, later “E. sibiricum” and “E. ursincola” were taxonomic transferred from this genus to new genera, Sandaracinobacter and Erythromonas, respectively, and validly published by Yurkov et al. in 1997. Tables 9.1 and 9.4 summarize the properties of Erythromicrobium ramosum and Croceicoccus marinus.
Genus Porphyrobacter Fuerst, Hawkins, Holmes, Sly, Moore and Stackebrandt (1993)
Porphyrobacter (Por.phy.ro.bac.ter. Gr. adj. porphyreos, purple; Gr. n. bacter, rod; M.L. masc. n. Porphyrobacter, porphyrinproducing rod, referring to bacteriochlorophyll production).
Cells are members of the α-subclass of Proteobacteria. They are Gram-negative, ovoid-to-short rods, pleomorphic, 0.5–1.0 × 0.5–2.8 μm, and reproduce by polar growth, budding, or asymmetric cell division. Colonies on complex media containing peptone are circular, smooth, opaque, and orange or red. They are neutrophilic freshwater bacteria, mesophilic to moderately thermophilic. Growth occurs at 10–60 °C, with an optimum temperature between 30 °C and 37 °C for most species. Cells are motile by peritrichous flagella or nonmotile. They are capable of producing structures that are multifibrillar stalk-like fascicles and crateriforms on the cell surface. Cells do not form any type of internal membranes. Spores and capsules are not formed. They are aerobic and chemoheterotrophic.
Cells synthesize BChl a on low-nutrient media under aerobic and semiaerobic conditions. Carotenoids are present. They are positive for calatase, d-glucose utilization, and hydrolyze of aesculine, but negative for citrate, l-arabinose, and d-fructose utilization. Cells do not grow phototrophically under anoxic conditions in the light. Simple organic compounds, peptone, and yeast extract are used as electron donors and carbon sources. Straight-chain octadecenoic acid (C18:1) is the major cellular fatty acid. 2-Hydroxy fatty acids and sphingoglycolipids are present, but 3-hydroxy fatty acids are absent. Ubiquinone-10 is the major quinine. Some strains may require vitamins for growth. The G+C of the DNA is 66.8–63.8 mol%.
Type species: Porphyrobacter neustonensis.
The genus currently contains six species with validly published names: P. neustonensis (Fuerst et al. 1993); P. tepidarius (Hanada et al. 1997); P. sanguineus (Ahrens 1968; Ahrens and Rheinheimer 1967; Hiraishi et al. 2002); P. cryptus (Rainey et al. 2003); P. donghaensis (Yoon et al. 2004b); P. dokdonensis (Yoon et al. 2006).
Tables 9.1 and 9.5 summarize the properties of the Porphyrobacter genus.
Isolation, Enrichment, and Maintenance Procedures
Members of this taxon have been isolated mainly from aquatic environments. However, there are also isolation reports from desert sand and rice in the Altererythrobacter genus. Growth media and culture conditions commonly used for the isolation of freshwater aerobic bacteria can be used for obtainment of Erythrobacteraceae members. Marine surface water, sediment, invertebrates, and freshwater environments are possible isolation sources for these organisms. MA and marine broth (MB) are the main culture media used to isolate and cultivate isolates. However, other media have been reported to be useful for isolation of Erythrobacteraceae members.
R2A (Difco) plates supplemented with 1 % NaCl and solidified with 1.5 % gellan have been used to isolate Altererythrobacter dongtanensis (Fan et al. 2011). Tryptone soy agar was used to isolate Altererythrobacter indicus (Kumar et al. 2008) and Altererythrobacter xinjiangensis (Xue et al. 2012).
R3A media solidified with agar (2 %, w/v) (Reasoner and Geldreich 1985; Williams and da Costa 1992) was used to isolate Porphyrobacter cryptus (Rainey et al. 2003). PE medium containing sodium glutamate, sodium succinate, sodium acetate, yeast extract, casamino acids, and a vitamin mixture (Hanada et al. 1995, 1997) supplemented with 1.5 % agar was used for isolation of Porphyrobacter tepidarius. Lake water agar (Franzmann and Skerman 1981) was used to isolate Polphyrobacter neustonensis (Fuerst et al. 1993). P. sanguineum strains were grown in MP medium, which consisted of marine broth and 0.5 % peptone water (1:1, vol/vol) (Hiraishi et al. 2002).
Erythromicrobium ramosum was isolated in a medium containing (per liter) 1.0 g of yeast extract, 1.0 g of bacto peptone, 1.0 g of sodium acetate, 0.3 g of KCl, 0.5 g of MgS04.7H20, 0.05 g of CaC12.2H20, 0.3 g of NH4Cl, 0.3 g of K2HP04, 20 pg of vitamin B12, and 1 ml of a trace element solution (Drews 1983; Yurkov et al. 1994). Croceicoccus marinus (Xu et al. 2009) was isolated by using ZoBell marine-casamino acids medium, which contained (per liter distilled water): NaCl, 19.45 g; MgCl2, 8.8 g; Na2SO4, 3.24 g; CaCl2, 1.8 g; KCl, 0.55 g; NaHCO3, 0.16 g; C6H5FeO7 . 5H2O, 0.1 g; KBr, 0.08 g; CsCl2, 34 mg; H3BO3, 22 mg; Na2SiO3, 4.0 mg; NaF, 2.4 mg; NH4NO3, 1.6 mg; Na3PO4, 8.0 mg; peptone, 0.5 g; yeast extract, 0.1 g; and casamino acids 0.1 g at a pH of 7.2 (ZoBell 1941).
Maintenance
It has been found that liquid cultures (taken from the late logarithmic growth phase) and agar surface cultures remained viable after storage at 4 °C for at least 2 months (Yurkov and Beatty 1998). Members of this family do not require special procedures for maintenance in medium and long-term storage. Strains may be preserved in screw-capped vials by freezing cell suspensions of liquid cultures or supplemented with MB (cultures mid-logarithmic growth phase) in 20 % (v/v) glycerol as a protective agent at −20 °C or at −70 °C. Long-term preservation is by lyophilization or by freezing cell suspensions in liquid nitrogen or at −80 °C in the presence of a cryoprotectant (Yurkov and Beatty 1998).
Physiological and Biochemical Features
Ecology
The habitat range of the family Erythrobacteraceae includes mainly aquatic environments. The original cultures were isolated from high-tidal seaweeds (Shiba and Simidu 1982), freshwater (Fuerst et al 1993; Yurkov et al 1994), cold-seep sediment (Kwon et al. 2007), and deep-sea sediment (Xu et al. 2009). This applies to most species described or reclassified recently. For instance, Erythrobacter marinus, E. pelagi, and Porphyrobacter dokdonensis were isolated from seawater (Yoon et al. 2006; Jung et al. 2012; Wu et al. 2012); Altererythrobacter dongtanensis and A. aestuarii were isolated from a tidal flat (Fan et al. 2011; Park et al. 2011), and A. ishigakiensis was isolated from marine sediment (Matsumoto et al. 2011). To date, all Erythrobacter species were retrieved from seawater environments, including marine invertebrates (E. vulgaris; Ivanova et al. 2006), as well as the monospecific Croceicoccus (C. marinus; Xu et al. 2009). The representative monospecific Erythromicrobium was isolated from freshwater (E. ramosum, Yurkov et al. 1994). Porphyrobacter genus includes members isolated from freshwater, brackish, and marine environments. To this genus belong isolates found in hot springs: P. tepidarius was isolated from a brackish hot spring (Hanada et al. 1997) and P. cryptus from a hot spring at Alcafache in central Portugal (Rainey et al. 2003). Both are moderately thermophilic. Altererythrobacter genus includes exceptions in addition to aquatic habitats: A. indicus, isolated from wild rice rhizosphere (Kumar et al. 2008) and A. xinjiangensis, isolated from desert sand (Xue et al. 2012).
The NCBI taxonomy browser Erythrobacter list includes isolates from a broader source than those of the type strains: marine aerosols (HQ188568); bacterioneuston (AY576736); coastal subseafloor (AB094461); soda pond (FN395246); biofilm on a copper-based antifouling paint (JN594622); Scrippsiella sp. laboratory culture (DQ486511); Dunhuang Mogao Grottoes 245# (JN244985); ancient salt deposits of the Yipinglang Salt Mine (EF177676); magnetite mine drainage (HQ652571); and chemocline of the hypersaline deep-sea Urania basin (AF321064).
The same search for Porphyrobacter resulted the following unusual sources: mine tailings ore and sand (JQ429465); an air sample collected 25 m above sea level (GQ484916); ozone-biological activated carbon filters for drinking water treatment (DQ884358); industrial site soil containing high amounts of heavy oil and heavy metals (HQ588835); Hamelin Pool stromatolites in Shark Bay, Australia (EF150743); aerobic fermentation of a mixture of bovine dung and urine, cow's milk, and yogurt (GQ246725); commercial nitrifying inoculum (AM236300); aquatic microbial mat from Antarctica (FR772128); arsenate resistant culture from estuary (AY788979); HAA degrading bacteria from drinking water (JN547328); oak (Quercus alba) leaf infusion (EF685171); ancient salt deposits of the Yipinglang Salt Mine (EF177679); and endophytic from a pine tree with Pine Wilt Disease (FJ784659). The NCBI taxonomy browser also includes P. meromictius isolated from a Na2SO4− dominated meromictic lake (Mahoney Lake in the Okanagan Valley of British Columbia, Canada) but the name is not valid (Rathgeber et al. 2007).
Erythromicrobium was found in mud volcano soil in Baratang Island, India (FN397674) and in arsenic-contaminated soil (AFI42455). The NCBI taxonomy browser also includes E. ezovicum and E. hydrolyticum, which are not valid names. These strains were reported to pertain to Vladimir Yurkov`s personal collection and were related to tellurite resistance and reduction (Yurkov et al 1996). Altererythrobacter has also been recovered from Polycyclic Aromatic Hydrocarbons (PAHs) and crude oil degrading consortia enriched from marine sediments (GQ505272); mud volcano soil in Baratang Island, India (FN397680); aquatic microbial mat from Antarctica (FR772131); root interior of Cymbidium goeringii (GQ476825); and farming field soil (JN848799).
The genera Erythrobacter, Porphyrobacter and Erythromicrobium include AAP members. AAPs contain BChl a as a main light-harvesting pigment; however, in contrast to purple nonsulfur photosynthetic bacteria, these are obligate aerobes (Yurkov and Beatty 1998). They are facultative photoheterotrophs, metabolizing organic carbon when available, but are capable of photosynthetic light utilization when organic carbon is scarce. The first AAP bacteria discovered was Erythrobacter longus (Shiba et al. 1979; Shiba and Simidu 1982). Porphyrobacter and Erythromicrobium members present BChl a (Yoon et al. 2006; Yurkov et al. 1994; Yurkov and Gorlenko 1993), whereas the Erythrobacter genus includes 2 species (out of 13) that synthesize BChl a: the former isolated E. longus retrieved from high-tidal seaweeds of Tokyo Bay (Shiba and Simidu 1982) and E. litoralis found in marine cyanobacterial mat in a supralitoral zone (Yurkov et al. 1994). It had been suggested that cultivated Erythrobacter species represent the predominant AAPs in the upper ocean and should be main players in carbon cycling in the ocean, mainly in the euphotic zone (Shiba et al. 1991; Fenchel 2001; Kolber et al. 2001; Karl 2002). Later, culture-independent genomic analyses targeting photosynthetic operon genes (i.e., pufM) showed dissimilar results. No sequences recovered in Monterey Bay waters or in the central North Pacific Ocean (Karl and Lukas 1996) were similar to those of Erythrobacter species (Béjà et al. 2002).
An extensive study included samples from the Pacific, Atlantic, and Indian Oceans and West Pacific marginal seas, including the East and South China Seas – covering tropical, subtropical, and temperate zones, as well as coastal, shelf, and oceanic waters; it was able to account Erythrobacter- and Roseobacter-like sequences for approximately a quarter of the totality sequences obtained in the study (Jiao et al. 2007). For nearshore/offshore samples from a Pacific Ocean transect, only one station (out of three) presented sequences (32 %) most similar to those from cultured Erythrobacter, but altogether with Rhodobacter and Roseobacter genera (Ritchie and Johnson 2012). It is now clear that Erythrobacter species are not the oceanic-dominating AAP population and the counterparts include a wide variety of bacterial types. Therefore, the relative contribution of Erythrobacter spp. to oceanic carbon cycling may not be as large as previously suggested. The studies quantify Bchl a, and it is widespread among a phylogenetically diverse group – the AAP bacteria – in which oceanic representation of Erythrobacter spp. is not a consensus and may be variable (Béjà et al. 2002; Rathgeber et al. 2004; Venter et al. 2004; Jiao et al. 2007; Yutin et al. 2007; Ritchie and Johnson 2012).
Pathogenicity: Clinical Relevance
No information on pathogenicity for members of Erythrobacteriaceae is available heretofore (as of February 2013). The detection of naturally occurring β-lactamases in Erythrobacter spp. gave rise to the idea that this group, as many other marine bacteria, plays an important role as reservoir of β-lactam resistance genes, namely the oceanic resistome. A beta-lactamase II from Erythrobacter litoralis HTCC 2594 (ELbla2) showing in silico similarity with New Delhi metallo-beta-lactamase (MBL) was expressed in E. coli cells. These two mature proteins were purified from cultures and both presented as a monomer of 25 kDa. Antimicrobial susceptibility assay revealed that both shared similar substrate specificities, being sensitive to aztreonam and tigecycline (Zheng et al. 2011). Further, several chromosomally located MBLs have been identified from Erythrobacter spp. by bioinformatic analyses followed by cloning and expressing in E. coli cells. These MBLs showed a large diversity and belonged to subclasses B1 or B3. None of them could be considered a progenitor of the plasmid-mediated carbapenemases disseminated worldwide.
Clones expressing the MBL from E. flavus and E. longus presented decreased sensitivity to carbapenems (Girlich et al. 2012). It was hypothesized that resistance genes are transferred to the human gut microbiota by means of the consumption of nonsterilized seafood (e.g., seaweeds) (Hehemann et al. 2010; Zheng et al. 2011), given that the virus-like gene transfer system identified, likely Gene Transfer Agent (GTA) systems, are common in marine bacteria (e.g., E. litoralis) (Biers et al., 2008), and that GTAs account for an horizontal gene transfer frequency that is a million times the frequencies of transformation and transduction (McDaniel et al. 2010).
Application
A summary of the main application properties for the Erythrobacteraceae members is presented in Table 9.10 .
Bioremediation
There are field and experimental evidences of the potential of Erythrobacteraceae members for bioremediation of heavy metals and a variety of xenobiotics, including hydrocarbons, aromatics and halogenates. For instance, Erythrobacter members were detected as part of the population related to alkane degradation from shoreline environments (Costa da Morte, Northwestern Spain) affected by the Prestige oil spill (Alonso-Gutiérrez et al. 2009). Erythrobacter longus and E. citreus were the closest phylogenetic neighbors related to the dominant clones identified after a bioremediated microcosm (nitrogen supplemented) experiment (Röling et al. 2002). A petroleum-aromatic-degrading active Altererythrobacter isolate is suggested to be a possible agent of bioremediation in and around nutrient-rich tropical marine environments (Teramoto et al. 2010). A Porphyrobacter strain, Oxy6 (according to 16S rRNA–based molecular phylogenetic analysis), isolated from subtropical Western Atlantic seawater, showed an ability to methyl halides degradation. This strain was even able to co-oxidize CH3Br while growing on toluene. A variety of toluene pathway intermediates, such as benzyl alcohol, benzylaldehyde, benzoate, and catechol, could also be oxidized. Furthermore, the bacterium also oxidized o-xylene and the xylene monooxygenase pathway intermediate 3-methylcatechol. Considering the widespread inhibitory effect of toluene on seawater samples and the substrate oxidation pattern of this Porphyrobacter sp., the authors suggested a possible link between aromatic hydrocarbon utilization and the biogeochemical cycle of methyl halides (Goodwin et al. 2005).
Erythrobacter and Erythromicrobium isolates demonstrated high-level resistance to tellurite and accumulation of metallic tellurium crystals. In Erythrobacter litoralis and Erythromicrobium ramosum isolates, crystals occupied 20–30 % of the cell volume. This reduction of tellurite to the relatively inert metallic tellurium [Te(IV) to Te(0)] with accumulation as intracellular deposits is suited to the development of microbiological methods for environmental remediation. Tellurite compounds are toxic to other bacteria and other organisms, including humans. Furthermore, bacterial cells can be harvested for pure tellurium metal in the mineral ore (Yurkov et al. 1996; Yurkov and Beatty 1998).
Carotenoids
A remarkable characteristic of many members of Erythrobactaeriaceae is the pigmentation (pink/red/orange/yellow) due to the production of carotenoids (Takaichi et al. 1988, 1990, 1991; Hanada et al. 1997; Yurkov et al. 1994; Denner et al. 2002; Xu et al. 2009). Erythrobacter longus produces approximately 20 different carotenoids, such as β-carotene and monocyclic carotenoids (e.g., rubixanthan) (Takaichi et al. 1990). The carotenoid biosynthesis genes lycopene cyclase (crtY) and phytoene desaturase (crtI), from E. longus strain Och101, were cloned, sequenced, and expressed in Escherichia coli. The E. coli HB101 employed contained the other required biosynthetic genes from Erwinia herbicola. Zeaxanthin and lycopene were produced and accumulated in the transformed cells, but transformants containing crtY and crtI genes from E. herbicola gave a higher pigment yield. The weak expression of E. longus crt genes in E. coli was attributed to codon usage bias (Matsumura et al. 1997).
Erythrobacter JPCC M sp. strain 1436 was included in a patent process for its astaxanthin productivity, reported to be 35 % or more by mass of the all produced pigments. According to 16S rDNA sequence similarity, the closest neighbor was Erythrobacter luteolus SW-109T (GenBank AY739662), with a low nucleotide identity of 95.7 %. Based on 16S rDNA phylogeny, the authors considered Erythrobacter JPCCM sp. strain 1436 (accession number NITE BP-340), a novel species belonging to the genus Erythrobacter, at the time of priority application (April 2007). The process was entitled “Astaxanthin-producing bacterium, bacterium culture product, astaxanthin-containing composition, and method for production of astaxanthin”; the European Patent Register Publication Number is EP 2157169 A1 (February 2010). The invention is claimed to be useful for the production of supplement foods and feedstuffs (color-enhancing feedstuffs).
Cytotoxic Compounds
Erythrobacter sp. strain SNB-035, isolated from mangrove sediments in Trinity Bay (Galveston, TX), yielded cytotoxic compounds: the benzothiazoles erythrazoles A-B and erythrolic acid D, a meroterpenoid. Cytotoxicity was observed against non-small cell lung cancer cell lines. Erythrazole B was cytotoxic, with IC50 values of 1.5, 2.5, and 6.8 μM against H1325, H2122, and HCC366, respectively. Erythrolic acid D was cytotoxic, with a modest IC50 value of 2.5 μM against HCC44. Strain SNB-035 shares 98 % 16S rRNA identity with E. citreus. (Hu and MacMillan 2011; Hu et al. 2012).
Light-Oxygen-Voltage Domains
Light-oxygen-voltage (LOV) domains are photosensory-signaling modules acting as blue light–dependent regulators of numerous activities, such as enzymes and DNA binding. LOV domains are widespread and highly conserved in eukaryotes, prokaryotes (including cyanobacteria), and archaeans; thus, they are suited for model-based studies. They can be readily produced in E. coli in amounts sufficient for biochemical and spectroscopic analysis. LOV domains can also be engineered into a variety of exogenous targets, allowing similar regulation for new protein-based reagents (Briggs et al. 2007; Möglich and Moffat 2010; Strickland et al. 2012). Erythrobacter litoralis presents the LOV-histidine kinase (LOV-HK) domain, which mediates light-activated histidine phosphorylation. E. litoralis strain HTCC 2594 has had full-length modules expressed in E. coli (EL346-LOV-HK and EL368-LOV-HK). The same was performed with modules from Brucella melitensis (animal pathogen) and Pseudomonas syringae (plant pathogen), allowing descriptive and comparative analysis (Swartz et al. 2007; Briggs et al. 2007; Tseng et al. 2010). EL222, a DNA-binding protein from the same E. litoralis strain, is also a model system. Despite its compactness (222 amino acids), it includes both sensor and effector domains. Nash et al. (2011) demonstrated that this LOV domain binds and inhibits a helix-turn-helix (HTH) DNA binding domain in the dark, releasing these interactions upon illumination. Furthermore, the same research group identified optimal DNA binding sites for EL222 and demonstrated the light-dependent activation of transcription (Fig. 9.4 ). EL222 LOV-HTH native targets are yet to be determined; nevertheless, the portability of the system, the direct regulation of DNA binding with light, together with the fact that the DNA binding sites are identified, make it attractive for engineering in heterologous systems (Rivera-Cancel et al. 2012).
Enzymes
Three epoxide hydrolases (EHases) genes (eeh1, eeh2, and eeh3) of Erythrobacter litoralis HTCC2594 were cloned in E. coli, and the recombinant proteins (rEEH1, rEEH2, and rEEH3) were purified. The functionality of purified proteins was proved by hydrolytic activities towards styrene oxide (SO). EEH1 preferentially hydrolyzed (R)-styrene oxide, whereas EEH3 preferred to hydrolyze (S)-SO, representing enantioselective hydrolysis of styrene oxide. EEH2 could hydrolyze (R)- and (S)-SO at an equal rate. The hydrolysis rate of EEH1 towards various epoxide substrates was superior to those of EEH2 or EEH3 (Woo et al. 2007). Erythrobacter sp. JCS358 also presents enantioselective epoxide hydrolyzing activity. Its performance was outstanding among marine strains isolated by the capability of living on SO and further screened for retaining enantioselective EHase activities towards SO (Hwang et al. 2008). Altererythrobacter epoxidivorans JCS350T was described as presenting EHase activity, but it was not reported if this activity was enantioselective (Kwon et al. 2007). Pharmaceutical industries are eager for enantioselective EHases for the production of enantiopure epoxides.
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Tonon, L.A.C., Moreira, A.P.B., Thompson, F. (2014). The Family Erythrobacteraceae. In: Rosenberg, E., DeLong, E.F., Lory, S., Stackebrandt, E., Thompson, F. (eds) The Prokaryotes. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-30197-1_376
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