Taxonomic hierarchy of the phylum Proteobacteria and Korean indigenous novel Proteobacteria species

Abstract

The taxonomic hierarchy of the phylum Proteobacteria was assessed, after which the isolation and classification state of Proteobacteria species with valid names for Korean indigenous isolates were studied. The hierarchical taxonomic system of the phylum Proteobacteria began in 1809 when the genus Polyangium was first reported and has been generally adopted from 2001 based on the road map of Bergey's Manual of Systematic Bacteriology. Until February 2018, the phylum Proteobacteria consisted of eight classes, 44 orders, 120 families, and more than 1,000 genera. Proteobacteria species isolated from various environments in Korea have been reported since 1999, and 644 species have been approved as of February 2018. In this study, all novel Proteobacteria species from Korean environments were affiliated with four classes, 25 orders, 65 families, and 261 genera. A total of 304 species belonged to the class Alphaproteobacteria, 257 species to the class Gammaproteobacteria, 82 species to the class Betaproteobacteria, and one species to the class Epsilonproteobacteria. The predominant orders were Rhodobacterales, Sphingomonadales, Burkholderiales, Lysobacterales and Alteromonadales. The most diverse and greatest number of novel Proteobacteria species were isolated from marine environments. Proteobacteria species were isolated from the whole territory of Korea, with especially large numbers from the regions of Chungnam/Daejeon, Gyeonggi/Seoul/Incheon, and Jeonnam/Gwangju. Most Halomonadaceae species isolated from Korean fermented foods and solar salterns were halophilic or halotolerant. Air-borne members of the genera Microvirga, Methylobacterium, and Massilia had common characteristics in terms of G+C content, major respiratory quinones, and major polar lipids.

Generally, the phylum Proteobacteria is known to be comprised of Gram-negative microorganisms, which have an outer membrane mainly composed lipopolysaccharides. Members of this phylum possess diverse characteristics morphologically, physiologically, ecologically, and pathogenically. A variety of cell shapes have been observed such as rods, stalks, buds, and filaments. Many species are motile by means of flagella, whereas some are non-motile or rely on gliding. Moreover, the species have various types of metabolic processes. Most members are facultatively or obligately anaerobic, chemolithoautotrophic, and heterotrophic, whereas some are autotrophic and perform photosynthesis (Imhoff and Hiraishi, 2005; Imhoff et al., 2005; Spieck and Bock, 2005). Members of this phylum are distributed across a wide range of habitats, including air, freshwater, seawater, soil, plants, animals, and acid mines. Furthermore, members include a wide variety of pathogens as well as nitrogen-fixing and predatory microorganisms. For this reason, the name Proteobacteria was chosen due to the group member’s diverse properties despite their common ancestry (Stackebrandt et al., 1988; Spain et al., 2009).

For the preservation of prokaryotic resources, a number of new bacterial species have been isolated from various environments in Korea, and the information on the novel species belonging to the phyla Actinobacteria (Bae et al., 2016) and Firmicutes(Seong et al., 2018) have been compiled.

The present work aimed to elucidate the chronological process of establishing a taxonomic hierarchy for the phylum Proteobacteria as well as the classifications of bacterial species belonging to this phylum isolated from Korean environments. In addition, we report the environmental and regional origins and the properties of the Proteobacteria isolates. A hierarchical taxonomic system of the phylum Proteobacteria was retrieved from the ‘Hierarchical classification of bacteria’ in the List of Prokaryotic Names with Standing in Nomenclature (LPSN; http:// www.bacterio.net/). Then, this system was compared with the ‘Taxonomy in NCBI database (https://www.ncbi.nlm. nih.gov/taxonomy)’. Finally, all names belonging to this phylum were checked by searching the ‘Notification list’ and ‘Validation list’ in the International Journal of Systematic and Evolutionary Microbiology (IJSEM; http://ijs. microbiologyresearch.org/). Data mentioned in this paper are limited to the Proteobacteria species validated until February 2018.

History of taxonomic hierarchy of the phylum Proteobacteria

The phylum Proteobacteria is the largest group in the domain Bacteria. Table 1 shows the periodic history of the phylum Proteobacteria, which was first proposed by Garrity et al. (2005) and authorized by the International Committee on Systematics of Prokaryotes (ICSP). A systematic history of the phylum Proteobacteria was first reported in 1809 by Link, who proposed the genus Polyangium with the type species P. vitellinum (Skerman et al., 1980). Successively, the genera Serratia (type species S. marcescens), Spirillum (type species S. volutans), Gallionella (type species G. ferruginea), Chromatium (type species C. okenii), Vibrio (type species V. cholerae), Crenothrix (type species C. polyspora), and Neisseria (type species N. gonorrhoeae) were proposed until 1885 (Skerman et al., 1980). After that, the higher taxa, family and order, were proposed along with the first family Crenotrichaceae (by Hansgirg in 1888) and first order Pseudomonadales (by Orla-Jensen in 1921) (Skerman et al., 1980). During that time, well-known taxa such as genera Rhizobium, Pseudomonas, Rickettsia, Escherichia, and Shigella as well as family Spirillaceae were created (Skerman et al., 1980).

Table 1. Establishment of hierarchical taxonomic system of the phylum Proteobacteria.

*¹⁾, Combined to Bradyrhizobiaceae; ²⁾, Combined to Nitrosomonadales; ³⁾, Shown in “Taxonomic outline”, Bergey’s manual of systematic bacteriology 2nd ed. (Garrity and Holt, 2001); ⁴⁾, Not listed on “Hierarchical classification of prokaryotes”, LPSN; ⁵⁾, Invalid name.

Abbreviations: Dm., domain; K., kingdom; Dv., division; P., phylum; C., class; O., order; F., family; G. genus; Cr., creation; Ex., exclusion; Pu., publication.

Meanwhile, in 1968, the kingdom Prokaryotae was created as the highest level of life and was appropriately at the same level as Eukaryotae (Gibbons and Murray, 1978). Its lower rank, the division Gracilicutes was created (Gibbons and Murray, 1978). The division name Gracilicutes represents thinner cell walls, implying a Gram-negative type of cell wall (Gibbons and Murray, 1978), and this division was further separated into the classes Photobacteria (containing subclasses Oxyphotobacteriae and Anoxyphotobacteriae) and Scotobacteria (for non-photosynthetic bacteria). Two other divisions, Firmicutes and Mollicutes, were also proposed to encompass Gram-positive bacteria and cell wall-lacking bacteria, respectively (Gibbons and Murray, 1978). Around this same time, Murray (1984) proposed that three classes, Scotobacteria (for non-photosynthetic bacteria), Anoxyphotobacteria (for photosynthetic bacteria having photosystem I alone), and Oxyphotobacteria (for bacteria having both photosynthetic systems I and II), be placed under the division Gracilicutes in Bergey’s Manual of Systematic Bacteriology (BSMB) 1st ed. In other words, the class Photobacteria was rearranged and divided into the two classes Anoxyphotobacteria and Oxyphotobacteria which is now classified as the phylum Cyanobacteria. Thus, members belonging to photosynthetic and other Gram-negative bacteria had been affiliated within the division Gracilicutes(Skerman et al., 1980) until 1988. The taxon name “division” was changed to “phylum” after the phylogenetic relationships were applied to the bacterial taxonomy (Woese, 1987).

With a higher rank than order, the class Proteobacteria was created under the division Gracilicutes in 1988 by Stackebrandt et al. (1988) in order to encompass the purple bacteria and their relatives. Moreover, the authors suggested to divide the class Proteobacteria into Alpha, Beta, Gamma, and Delta groups at the subclass level. In 1990, the domain Bacteria was created as a higher rank of the kingdom Prokaryotae, which was excluded in 1994 (Woese et al., 1990; Embley et al., 1994). Members of the classes Scotobacteria and Proteobacteria were reclassified and moved to the new classes Acidobacteria and Chlamydiae or phyla such as Cyanobacteria, Chloroflexi, Plantobacteria, and Spirochaetae (Garrity and Holt, 2001; Cavalier-Smith, 2002). Finally, the phylum Proteobacteria was created with its lower rank, classes Alpha-, Beta-, Delta-, Epsilon-, and Gammaproteobacteria, which was listed in Bergey’s Manual of Systematic Bacteriology (Garrity et al., 2005). At that time, 28 orders were proposed: 27 orders in BSMB 2nd ed. and order Kordiimonadales by Kwon et al. (2005). Members of Cytophaga, Flavobacteria, and Sphingobacteria, previously affiliated within the class Scotobacteria, were moved to the phylum Bacteroidetes which was created in 2011 (Krieg et al., 2011). Consequently, a hierarchical classification system of the phylum Proteobacteria was generally adopted starting in 2011. Recently, four new classes, Acidithiobacillia (from Gammaproteobacteria; Williams and Kelly, 2013), Oligoflexia (Nakai et al., 2014), “Zetaproteobacteria” (Makita et al., 2017), and Hydrogenophilalia (from Betaproteobacteria; Boden et al., 2017), and 13 new orders were proposed: Emcibacterales, Iodidimonadales (Iino et al., 2016), Magnetococcales (Alphaproteobacteria; Bazylinski et al., 2013), Bradymonadales (Deltaproteobacteria; Wang et al., 2015c), Enterobacteriales (Adeolu et al., 2016), Acidiferrobacterales(Kojima et al., 2015), Arenicellales (Teramoto et al., 2015), Cellvibrionales (Spring et al., 2015), Nevskiales (Naushad et al., 2015), Orbales (Gammaproteobacteria; Kwong and Moran, 2013), Oligoflexales (Nakai et al., 2014), Bacteriovoracales(Hahn et al., 2017), and Silvanigrellales(Oligoflexia; Hahn et al., 2017).

As of February 2018, the phylum Proteobacteria consisted of nine classes comprising 56 orders, 155 families, and 1,084 genera. In this work, the following taxa were included categorized in one of the following statuses: 1) validated but not shown in the ‘Hierarchical classification of prokaryotes (LPSN)’ and 2) listed in the ‘Taxonomy (NCBI) database’ but listed in quotes on the ‘Hierarchical classification of prokaryotes (LPSN)’. These taxa are as follows: three classes, Acidithiobacillia, Hydrogenophilalia, and “Zetaproteobacteria”, the orders Enterobacterales (Adeolu et al., 2016), Immundisolibacterales (Corteselli et al., 2017), Emcibacterales, Iodidimonadales (Iino et al., 2016), Micropepsales(Harbison et al., 2017), Rhodothalassiales(Venkata Ramana et al., 2013), “Mariprofundales”, “Parvularculales”, “Procabacteriales”, and “Vibrionales”, and the families Erwiniaceae, Pectobacteriaceae, Yersiniaceae, Hafniaceae, Morganellaceae, Budviciaceae (Adeolu et al., 2016), Thorselliaceae (Kämpfer et al., 2015), Micropepsaceae (Harbison et al., 2017), Chelatococcaceae (Dedysh et al., 2016), Mabikibacteraceae (Choi et al., 2017), Notoacmeibacteraceae (Huang et al., 2017), Rhodothalassiaceae, Vulgatibacteraceae, Labilitrichaceae, Anaeromyxobacteraceae (Yamamoto et al., 2014), Wenzhouxiangellaceae (Wang et al., 2015b), Immundisolibacteraceae (Corteselli et al., 2017), Kangiellaceae (Wang et al., 2015a), Ventosimonadaceae (Lin et al., 2016), Fastidiosibacteraceae (Xiao et al., 2018), “Salinisphaeraceae” (Naushad et al., 2015), “Mariprofundaceae”, “Parvularculaceae”, “Kordiimonadaceae”, “Aurantimonadaceae”, “Procabacteriaceae”, “Hydrogenimonaceae”, and “Saccharospirillaceae”.

On the other hand, the orders Holosporales, Kopriimonadales, Pelagibacterales, Ferritrophicales, Ferrovales, and Salinisphaerales and the families Pelagibacteraceae, Geminicoccaceae, Ferritrophicaceae, and Ferrovaceae which appeared in the NCBI database were not included due to the lack of validation. Moreover, the orders Methylophilales and Sulfuricellales were not included since these orders were combined into the order Nitrosomonadales (Boden et al., 2017). The order Xanthomonadales and its family Xanthomonadaceae were excluded since the names Lysobacterales and Lysobacteraceae have priority over those names, respectively. The families Haliangiaceae and Sinobacteraceae were also excluded since families Kofleriaceae and Nevskiaceae have priority over those names, respectively (Tindal, 2014).

Novel species belonging to the phylum Proteobacteria originating from Korea

Efforts to name the Proteobacteria isolates from Korea began in 1999 using the species Erwinia pyrifoliae for plant-pathogenic isolates obtained from Asian pear tree (Kim et al., 1999). Since then, many new Proteobacteria species have been recorded with valid names. In February 2018, 644 Proteobacteria species originating from Korea were approved (Table 2).

Table 2. List of novel Proteobacteria species with valid name originated from Korea.

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*Numerals in the parentheses are the number of species. †Denotes the creation of the genus, family, and order. Abbreviations of the source: ai, air and air-conditioning system; co, compost; cu, culture in lab.; ds, deep sea sediment; fa, freshwater algae; ff, fermented food; fs, freshwater sediment; fw, freshwater; ma, marine animal; mp, marine plant or seaweed; py; terrestrial plant, sl, solar saltern and salt lake; sr, soil without vegetation or contaminated soil; ss, seashore sand; sv, soil with vegetation (agricultural and forest); sw, seawater; ta, terrestrial animal; tf, tidal flat sediment; wc, water cooling or purifying system; ww, wastewater. Abbreviations of the Table 2. region: AR, artificial environment; CB, Chungbuk; CD, Chungnam/Deajeon; UD, Ulreung and Dokdo islands; GBU, Gyeongnam/Busan/Ulsan; GD, Gyeongbuk/Daegu; GSI; Gyeonggi/Seoul/Incheon; GW, Gangwon; JB, Jeonbuk; JG, Jeonnam/Gwangju; JJ, Jeju; UN, site unspecified; WS, 5 West sea islands. Abbreviations of the function: ¶a, Aliphatic hydrocarbon degradation; ¶b, Aromatic hydrocarbon degradation; ¶c, Herbicide degradation; ¶d, Poly

All Proteobacteria species are affiliated within four classes (Alpha-, Beta-, Epsilon-, and Gamma-proteobacteria), 25 orders, 65 families, and 261 genera (including 10 genera of which families were unassigned). A total of 304 species belong to the class Alphaproteobacteria, 257 species to the class Gammaproteobacteria, 82 species to the class Betaproteobacteria, and one species to the class Epsilonproteobacteria.

Composition of novel species belonging to the class Alphaproteobacteria: Novel Korean isolates belonging to the class Alphaproteobacteria were affiliated with 129 genera and 23 families within eight orders. A total of 129 species were affiliated with the order Rhodobacterales, 77 species with Sphingomonadales, 42 species with Rhizobiales, 25 species each with Rhodospirillales and Caulobacterales, and the remaining six species were affiliated with the orders Kiloniellales, Kordiimonadales, and Sneathiellales or with an order unassigned. In the order Rhodobacterales, all species were included in 64 genera belonging to the single family Rhodobacteraceae. The genera Paracoccus (11 species), Loktanella (10 species), Roseovarius(10 species), Jannaschia (seven species), Sulfitobacter (six species), Litoreibacter (five species), and Ruegeria (five species) encompassed five or more Korean novel species. Fifty-six species belonging to 10 genera were affiliated with the family Sphingomonadaceae, and 21 species belonging to three genera were with the family Erythrobacteraceae of the order Sphingomonadales. A number of isolates were affiliated with the Sphingomonadaceae genera Sphingomonas (29 species) and Sphingopyxis (10 species) as well as the two Erythrobacteraceae genera Altererythrobacter and Erythrobacter(nine species each). Forty-two species belong to 24 genera within 13 families in the order Rhizobiales. The family Rhizobiaceae contained 11 species while one of its genera, Kaistia, contained six species. The genera Devosia and Methylobacterium within the families Hyphomicrobiaceae and Methylobacteriaceae, respectively, contained five species each. Twenty six Rhodospirillales species were distributed within two families, Acetobacteraceae (12 species within four genera) and Rhodospirillaceae (nine species within eight genera), with four species (one genus) of which the family unassigned. The genus Roseomonas of the family Acetobacteraceae contained nine novel Korean species.

In the order Caulobacterales, 25 novel Korean isolates were affiliated with two families Caulobacteraceae (15 species within four genera) and Hyphomonadaceae (10 species within eight genera).

Composition of novel species belonging to the class Betaproteobacteria: Betaproteobacteria isolates were affiliated with only three orders, Burkholderiales(73 species), Neisseriales(seven species), and Rhodocyclales(two species). Seventy-three Burkholderiales isolates consisted of 23 Comamonadaceae species (11 genera), 17 Burkholderiaceae species (four genera), 15 Oxalobacteraceae species(four genera), 13 Alcaligenaceae species, and five species(five genera) of which the family was unassigned. All seven Neisseriales species were affiliated with seven different genera of the family Chromobacteriaceae. Only two species (two genera) belonged to the family Zoogloeaceae within the order Rhodocyclales. The genera Burkholderia (11 species) and Massilia (10 species) within the families Burkholderiaceae and Oxalobacteraceae of the order Burkholderiales, respectively, were dominant.

Composition of novel species belonging to the class Gammaproteobacteria: Ten orders were detected in the class Gammaproteobacteria; Lysobacterales (73 species), Alteromonadales (65 species), Oceanospirillales (39 species), Pseudomonadales (23 species), Cellvibrionales (20 species), Chromatiales (seven species), Nevskiales (six species), Legionellales, Orbales, Thiotrichales (one species each), and an order unassigned (four species). Forty-five species(eight genera) and 28 species(eight genera) belonged to two Lysobacterales families, Lysobacteraceae and Rhodanobacteraceae, respectively. Twenty-three, eight, and five novel species were affiliated with the genera Lysobacter, Pseudoxanthomonas, and Arenimonas of the family Lysobacteraceae, respectively. Moreover, 12 and eight species belonged to Rhodanobacter and Dyella of the family Rhodanobacteraceae, respectively. Sixty-five Alteromonadales species were distributed into 20 genera within nine families. Among them, a larger number of isolates belonged to the families Alteromonadaceae (31 species within 11 genera) and Shewanellaceae (13 species within one genus). The genera Shewanella (13 species; Shewanellaceae), Marinobacter (seven species), Marinobacterium (six species; Alteromonadaceae), and Idiomarina (five species; Idiomarinaceae) were the most abundant groups. Oceanospirillales isolates were composed of seven families (18 genera), including the abundant family Halomonadaceae (14 species within four genera). Eleven Halomonas (Halomonadaceae) species were isolated from Korean environments. The two families Moraxellaceae (15 species within four genera) and Pseudomonadaceae (eight species within the single genus Pseudomonas) were found in the order Pseudomonadales. Seven species were affiliated with the genus Psychrobacter of the family Moraxellaceae. Twenty Cellvibrionales species were distributed into five families, including the abundant family Cellvibrionaceae (10 species within six genera). Six species were placed in the genus Microbulbifer of the family Microbulbiferaceae. In addition, remaining Gammaproteobacteria isolates were affiliated with the orders “Vibrionales” (11 species, three genera, single family), Chromatiales(seven species, three genera, three families), Nevskiales (six species, four genera, two families), Aeromonadales (four species, two genera, single family), ‘Enterobacteriales’(two species, two genera, two families), Legionellales, Orbales, Thiotrichales (one species each), and an order unassigned (four species, three genera). Among them, the genera Photobacterium (six species; Vibrionaceae) and Rheinheimera (five species; Chromatiaceae) were dominant.

Composition of the novel species belonging to the class Epsilonproteobacteria: Only one Arcobacter species was affiliated with the family Campylobacteraceae, the order Campylobacterales within the class Epsilonproteobacteria.

New genera or higher taxa: The order Kordiimonadales within the class Alphaproteobacteria (Kwon et al., 2005) and three families, Cohaesibacteraceae (Hwang and Cho, 2008) and Mabikibacteraceae (Choi et al., 2017) of the order Rhizobiales and Litoricolaceae (Kim et al., 2007) of the order Oceanospirillales, were first created using isolates from the Korean environment as a type genus and species. Unfortunately, the family name “Kordiimonadaceae” was not validly published. In addition, 86 genera were first created using isolates from the Korean environment as the type species. Among them, 42 genera consisted of only a single type species(Table 2).

Researcher, isolation source, regional origin, and properties of species

Researchers: Eighty-one corresponding authors were involved in the proposal of novel species from the Korean indigenous Proteobacteria isolates. Among them, 15 corresponding authors proposed 488 novel species; Yoon, J. H.(172 species; Sungkyunkwan University), Kwon, S. W. (60 species; Rural Development Administration), Jeon, C. O.(42 species; Chung-Ang University ), Bae, J. W.(33 species; Kyung Hee University), Lee, S. T. (30 species; KAIST), Seong, C. N. (19 species; Sunchon National University), Lee, T. H. (18 species; Kyung Hee University), Cho, B. C. (17 species; Seoul National University), Chun, J.(16 species; Seoul National University), Im, W. T. (16 species; Hankyoung National University), Kim, J.(15 species; Kyeonggi University), Yang, D. C. (14 species; Kyung Hee University), Cho, J. C. (14 species; Inha University), Chung Y. R. (12 species; Gyeongsang National University), and Lee, S. D. (10 species; Jeju National University).

Isolation sources: Proteobacteria species from Korea were isolated from natural environments such as soil, freshwater, seawater, tidal flat sediments, air, and solar salterns, and a number of species were also isolated from artificial sources such as fermented foods, wastewater, compost, air conditioning systems, and water purifying systems. Several species were associated with animals and plants. Isolation sources of the species are described in detail. A total of 171 species were isolated from soil, including cultivated fields, forest soil, rhizosphere, natural caves, and reclaimed soil. Moreover, seawater (130 species) and tidal flat sediments (118 species) were the main isolation sources for Proteobacteria. Other major isolation sources were as follows: marine animals(32 species), wastewater(31 species), seashore sand (30 species), freshwater (27 species), air and air conditioning systems (22 species), solar salterns (19 species), and freshwater sediments(16 species). In addition, there were many other isolation sources for Proteobacteria species: Korean traditional fermented foods (jeotgal and kimchi; eight species), terrestrial plants(eight species), marine seaweed (seven species), laboratory cultures(seven species), compost (six species), insect gut (five species), water cooling or purifying systems(four species), freshwater algae (two species), and deep sea sediments(one species). Compared to the isolation sources of novel Actinobacteria and Firmicutes species, Proteobacteria species were isolated more frequently from marine environments such as seawater, tidal flat sediments, marine animals, seashore sand, and air/air conditioning systems but less frequently from Korean traditional fermented foods and clinical specimens(Bae et al., 2016; Seong et al., 2018).

Regional origin of the isolates: Novel Proteobacteria species were isolated from the whole territory of Korea. Predominant isolation regions of validly named Proteobacteria species were as follows (Table 2): 129 species from Chungnam/Daejeon (80 genera, 33 families, 15 orders, and three classes), 120 species from Gyeonggi/ Seoul/Incheon (75 genera, 32 families, 15 orders, and three classes), 72 species from Jeonnam/Gwangju (54 genera, 24 families, 14 orders, and three classes), 60 species from Gyeongnam/Busan/Ulsan (47 genera, 19 families, 13 orders, and three classes), 58 species from Jeju (43 genera, 25 families, 14 orders, and three classes), 34 species from Gwangwon (31 genera, 17 families, 11 orders, and three classes), 30 species from Gyeongbuk/Daegu (26 genera, 17 families, 11 orders, and three classes), 30 species from Jeonbuk (23 genera, 16 families, 10 orders, and three classes), and 25 species from Ulreung-/Dok-do Islands(23 genera, 19 families, 12 orders, and four classes). Since 26 species (20 genera, 15 families, 10 orders, and three classes) were isolated from artificial environments such as fermented foods, wastewater treatment systems, and air conditioning systems, their regional origins were not exactly specified. Moreover, regarding the 42 species (33 genera, 20 families, 11 orders, and three classes) from natural environments, their isolation regions could not be obtained.

Properties of the novel species: Isolates from soil, freshwater, seawater, and tidal flat sediments of Korea were affiliated with many genera. However, several taxa had co-relationships with isolation sources. In particular, some species were mainly isolated from marine-related environments such as seawater, tidal flat sediments, marine animals, and solar salterns: families Erythrobacteraceae, Kordiimonadaceae, and Rhodobacteraceae of the class Alphaproteobacteria as well as Vibrionaceae, Aeromonadaceae, Alteromonadaceae, Colwelliaceae, Idiomarinaceae, Pseudoalteromonadaceae, Shewanellaceae, Cellvibrionaceae, Microbulbiferaceae, Chromatiaceae, “Saccharospirillaceae”, Hahellaceae, Halomonadaceae, Kangiellaceae, and Oceanospirillaceae of the class Gammaproteobacteria. In particular, 10 out of 14 Halomonadaceae species were isolated from solar salterns and fermented foods. Moreover, these Halomonadaceae species were halophilic or halotolerant; in particular, Halomonas taeanensis(Lee et al., 2005) and Halomonas jeotgali(Kim et al., 2010) could grow at 25% NaCl(w/v). Compared to Korean novel bacterial species of other phyla, these Halomonas species were less halophilic than the Firmicutes species such as Lentibacillus kimchii(Oh et al., 2016) and Virgibacillus alimentarius (Kim et al., 2011) but more halophilic than the Actinobacteria species such as Nocardiopsis kunsanensis (Chun et al., 2000) and Kocuria koreensis (Park et al., 2010) as well as the Bacteroidetes species such as Salegentibacter salinarum (Yoon et al., 2008) and Psychroflexus salinarum (Yoon et al., 2009).

Members of the families Caulobacteraceae, Rhizobiaceae, Alcaligenaceae, Burkholderiaceae, Chromobacteriaceae, and Rhodanobacteraceae were mainly isolated from the terrestrial environment such as cultivated soil, freshwater, and wastewater.

Moreover, both Microvirga species and three out of five Methylobacterium species of the family Methylobacteriaceae, order Rhizobiales and five out of 10 Massilia species of the family Oxalobacteraceae, order Burkholderiales were isolated from air samples. The members of the genera Methylobacterium, Microvirga, and Massilia had common characteristics; high G+C content over 60 mol%, ubiquinone -8 or -10 as a major respiratory quinone, and phosphatidylethanolamine, phosphatidylglycerol, and diphosphatidylglycerol as major polar lipids.

Several novel Proteobacteria species from Korean environments showed specific functions such as degradation of polysaccharide, protein, lipid or hydrocarbon, and pesticide, and production of bile acid, high-pressure cold-adapted molecule, and antibiotics. Also, some species were involved in the nitrogen cycle with nitrogen fixation, denitrification or nitrate-reduction (Table 2).

Finally, a large number of novel Proteobacteria species are being isolated since researchers are aiming to find novel strains from extreme or untapped environments and by using new cultivating methods(Yang et al., 2007; Altankhuu and Kim, 2017).