Summary

Raoultella genus consists of Gram-negative, aerobic, encapsulated and non-motile rods. The name of the genus derives from the name of the French bacteriologist Raoul. Currently, four species belong to the genus: R. planticola, R. ornithinolytica, R. terrigena and R. electrica. The standard biochemical test used to identify Raoultella genus should be supplemented with additional tests, because of the close relationship between the genera Raoultella and Klebsiella. In 2001 Klebsiella planticola, K. ornithinolytica and K. terrigena were re-classified to new genus Raoultella. Re-classification was based on 16S rRNA sequence and rpoB, gyrA and gyrB genes. An alternative to phenotypic identification may be mass spectrometry or genetic methods (16s rRNA). These bacteria are commonly associated with natural environments (plants, water, soil). Raoultella spp. rods are not a highly virulent pathogen. Their virulence factors include polysaccharide capsule, fimbriae, siderophores, toxins and ability to form a biofilm. It has been shown that Raoultella spp. may colonize the gastrointestinal and upper respiratory tract in humans and cause cholangitis and lung infections. The literature also includes works on the antimicrobial activity of Raoultella rods and the possibility of using them in the environment protection. This review summarizes the current knowledge of Raoultella species identification, virulence and the possibility of using them in the protection of the environment.

Introduction

Raoultella spp. are Gram-negative, encapsulated, short rods of the Enterobacteriaceae family. Raoultella spp. belongs to non-motile and non-spore forming bacteria, primarily isolated from the natural environment [14, 23, 31, 44]. They are catalase-positive and oxidase-negative. All Raoultella spp. strains ferment glucose and lactose. Most strains ferment glucose forming acid and gas. The main product of glucose fermentation is 2,3-butanodiol. Those bacteria, like other Enterobac­teriaceae, reduce nitrates to nitrites. Raoultella spp. are facultative anaerobes capable of growing at the temperature range from 4°C to 40°C. They have low nutritional requirements and can grow on simple media. Most Raoultella spp. strains grow on solid media in the form of mucous colonies, which is related to the forming of polysaccharide capsules [44] (Fig. 1).

Fig. 1. R. ornithinolytica culture on MacConkey Agar

Since the time of their discovery, Raoultella spp. have been regarded as an environmental infection-causing bacteria, which has rarely been isolated from patients. Although they do not belong to well-recognized human pathogens, Raoultella spp. receive much attention from microbiologists because they increasingly more often cause bacteremia, cholangitis and pneumonia [49]. The best-described species is R. planticola, which is also most frequently isolated from infections in humans. The growing interest in Raoultella is not only connected with the increasing frequency of isolation from clin­ical specimens, but also from the introduction of new diagnostic methods that enable reliable identification of those bacteria with respect to genus and species. Reports published concern the biology of these bac­teria, their occurrence in water, food and their potential use in environmental protection.

History, classification and identification of Raoultella

The history of Raoultella genus is very complex. In 1977, Gavini et al. [19] suggested that Klebsiella strains isolated from the natural environment belonging to J, K, L and 
M groups should be described with the common name “Klebsiella-like organisms”. In the 1980s, the species names K. planticola [3], K. terrigena [22] and K. ornithinolytica [48] were introduced for these bacteria. In 1983, Ferragut et al. [14] discovered the fourth species – K. trevisanii. Three years later, Freney et al. [18] included the latter into the species – K. planticola, based on homology to the species 
K. planticola and K. trevisanii. In 2014 Kimura et al. [25] published an article about a new species R. electrica.

In 2001, Drancourt et al. [12] re-classified Klebsiella species isolated from the natural environment to a new genus Raoultella. Re-classification was based on 16S rRNA sequence and rpoB, gyrA and gyrB genes.

Biochemical identification remains the most frequently used method for bacteria identification in many microbiological laboratories. Because of the close relationship between the genera Raoultella and Klebsiella, biochemical tests normally used in microbiological laboratories often do not allow them to be distinguished. Therefore, differentiation of those genera is largely based on 
biochemical reactions unavailable in commercial diagnostic tests. Raoultella spp. use histamine and 3-DL-beta-hydroxybutyric acid as the only source of carbon in the medium, whereas Klebsiella spp. use ethanolamine. The use of 3-DL-beta-hydroxybutyric acid as the only source of carbon is also characteristic of K. pneumoniae and 
K. rhinoscleromatis strains. Studies of various authors [21, 30, 56] confirm that additional biochemical reactions, i.e. the use of histamine, ethanolamine and 3-DL-beta-hydroxybutyric acid as the only source of carbon in the medium, enables identification of Raoultella rods at genus, and sometimes at species level. Raoultella spp. strains can grow at 10°C, similarly to K. oxytoca strains. Unlike rods from Klebsiella genus, Raoultella grow at 4°C and do not produce gas from lactose at the temperature of 44.5°C [13, 56]. The differentiation of Raoultella spp. is based mostly on the use of D-melezitose as the only source of carbon in the medium by R. terrigena strains, the ability to grow at 42°C for R. planticola and R. ornithinolytica and production of ornithine decarboxylase by the strains of R. ornithinolytica. As shown in Table 1, the three species within the genus may be distinguished based on their characteristic biochemical profiles.

Biochemical profile	R. planticola	R. ornithinolytica	R. terrigena
Voges-Proskauer test	+	+	+
Lysine decarboxylase	+	+	+
Histidine decarboxylase	V	+	–
Phenylalanine deaminase	–	–	–
β-galactosidase	+	+	+
b-glucosidase	+	+	+
5-Keto-D-gluconate	+	+	+
Indole production	V	+	–
Citrate utilization	+	+	+
Malonate utilization	+	+	+
Fermentation of D-glucose at 44.5°C	–	–	–
Fermentation of D-turanose	V	V	V
Fermentation of β-gentiobiose	+	V	+
Fermentation of L-sorbose	+	+	V
Fermentation of L-rhamnose	+	+	+
Fermentation of L-fucose	+	+	+
Lipase (corn oil) activity	–	–	–
Gelatin hydrolysis (22°C)	–	–	–
Gas formation from lactose at 44.5°C	–	–	–
Utilization of hydroxy-L-proline	+	+	V
Growth in KCN presence	+	+	+
H2S production	–	–	–
Urea hydrolysis	+	+	–
Pectate degradation	–	–	–
Methyl red test	V	+	+
Utilization of m-hydroxybenzoate	–	–	+

Table 1. Biochemical profiles of Raoultella species

Identifying Raoultella rods concerning both genus and species is very difficult. Liu et al. [29] claim that strains earlier identified as K. oxytoca may belong to the species R. planticola. This was based on a PCR analysis of beta-lactamases genes and beta-lactamases isoelectric points values.

Genetic methods, based on the analysis of 16S rRNA, rpoB gene or hdc gene may be an alternative to the biochemical identification of Raoultella spp. [12, 20, 37, 45, 55], as well as mass spectrometry [10, 33, 45, 46], analysing the unique protein profile of the bacteria, referred as a molecular “fingerprint”. Risch et al. [46] identified Raoultella by mass spectrometry and confirmed identification by 16SrRNA sequencing. Ponce-Alonso et al. [45] correctly identified 11 Raoultella species by MALDI-TOF (score 2.35-2.50) and rpoB sequencing, whereas 16S rRNA provided inconclusive results. The authors in the MALDI-TOF MS method obtained identification score 
≥ 2.35 for all R. ornithinolytica and R. planticola strains. In turn, de Alegria Puig et al. [9] identified 97 Raoultella strains by mass spectrometry: Vitek MS and Bruker Biotyper. The authors obtained sensitivity 98.9 and 57.9%, and specificity 98.9 and 37.0%, respectively. Earlier studies confirm the effectiveness of the MALDI TOF method in the identification of Raoultella in terms of the genus and species [10, 46, 49]. In turn, Ponce-Alonso et al. [45] suggested sequencing specific genes: blaORN in R. ornithinolytica strains and blaPLA in R. planticola strains as reference method for identification of Raoultella strains. The authors detected blaORN gene in all of analyzed R. ornithinolytica strains and blaPLA gene in R. planticola strains.

Virulence factors of Raoultella spp.

Raoultella genus is not a highly virulent pathogen. The virulence factors of these bacteria are similar to Klebsiella rods (Table 2). Like other Gram-negative bacteria, Raoultella have a lipopolysaccharide (LPS) localized in the outer membrane. LPS is responsible for the biolo­gical activity of endotoxins, which are of key importance in the systemic infections [44]. LPS consists of three parts: the somatic antigen (O-antigen), the core and lipid A. O antigen are built out of repeating saccharide chains. This is the most immunogenic factor, determining the 
O serotype of the bacteria [44]. Leone et al. [27] detected a characteristic linear tetrasaccharide containing cyclic aceto-pyruvic acid in R. terrigena. Pillon et al. [39], analysing the composition of exopolysaccharide in R. terrigena, detected a pentasaccharide composed of repeating subunits of galactose, glucose, mannose and glucuronic acid in a ratio of 1:2:1:1.

Virulence factor	Species
LPS, O-antigen	R. planticola, R. terrigena, R. ornithinolytica
Serum resistance	R. planticola, R. terrigena
Polisaccharide capsule, K antigen	R. planticola
Adhesins (type 1 fimbriae, type 3 fimbriae)	R. planticola, R. terrigena
Siderophores (enterobactin, aerobactin)	R. planticola, R. terrigena, R. ornithinolytica
Ability to form biofilm	R. planticola, R. terrigena
Toxins, tetrodotoxin	R. terrigena
Bacteriocins, raoultellin L	R. terrigena, R. ornithinolytica

Table 2. Virulence factors of Raoultella species

Like in the case of Klebsiella spp., the polysaccharide capsule is the essential virulence factor of bac­teria from Raoultella genus. It protects the bacteria from phagocytosis [41]. Raoultella spp. typing based on capsular antigen was conducted by Podschun et al. [41, 42]. They detected this antigen in 96% strains of R. planticola. According to the cited authors, the most often identified antigens were: K14 (13.0%), K2 (9.0%) and K70 (9.0%). Antigen K70 it is common for R. planticola species. No work was found in the currently available literature where the authors would detect this (K70) serotype in strains of the genus Klebsiella. Strains with antigen K2 is regarded as more virulent than strains with the other serotypes [43]. The study of Podschun et al. [43] concerning R. planticola strains isolated from water indicate that highly virulent strains of K2 serotype can also be isolated from the natural environment.

The ability to form biofilm is also likely to be of vital importance in the infections caused by Raoultella spp. [35]. Participation in forming multispecies biofilm was confirmed for strains of R. planticola and R. terrigena. It was proven that these bacteria could produce large amounts of an exopolysaccharide, essential for the bacteria survival in the biofilm structure [35]. The biofilm is formed by adjoining cells of the microorganism surrounded by the extracellular matrix. One of the stages of biofilm production is the adhesion, which involves fimbriae. Podschun et al. [43] list fimbriae as one of the virulent factors. These are structures responsible for the adhesion of bacterial cells to the host cells. They allow adhesion, which facilitates the colonization of the host mucous membranes, often enabling the development of the infection. According to Podschun et al. [41], mannose-sensitive type 1 fimbriae occur in 83.0% of R. planticola strains, mannose-resistant type 3 in 69.0%, and 4.3% of the strains do not have fimbriae. Type 1 and 3 fimbriae are crucial for adhesion to the epithelial cells of the urinary, respiratory and digestive tracts.

Bacterial ability to survive in the host tissues is limited not only by the host defensive mechanisms but also by the limited availability of iron, which is necessary for bacterial growth. The ability to form siderophores, structures which enable bacteria to take up iron, necessary for life processes, was detected in strains of R. planticola. R. planticola can produce two types of siderophores: enterobactin (100% strains) or aerobactin (only 2.2% of strains) [43]. The ability to produce siderophores was also confirmed for 81.8% strains of R. ornithinolytica [2].

Many of the Gram-negative bacteria strains are sensitive to the bactericidal effect of human serum, whereas patho­genic strains often exhibit serum resistance properties [36]. Podschun et al. [42] also reported the resistance of R. planticola strains to the bactericidal effect of serum. They indicated that there is a relationship between the strain isolate and this property. Interestingly, this property seems to be more expressed in clinical strains than in those isolated from the natural environment. Of the 92 clinical strains, 30.4% were resistant to serum, whereas, among the strains cultured from water, only less than 4% showed this trait [43].

Little is known about toxins synthesized by Raoultella. Yu et al. [59] described the ability to produce tetrodotoxin by R. terrigena strains. Poisoning appeared after consumption of the pufferfish. This toxin is one of the most fatal neurotoxins. Bacteria producing tetrodotoxin were isol­ated from different marine organisms, mostly from fish Takifugu and Fugu. Tetrodotoxin can be accumulated in different organs of the fish, mostly in the skin, intestine, liver and ovaries. The ability to synthesize this toxin was also confirmed in other bacteria, e.g., Pseudomonas, Vibrio, Aeromonas, Shewanella, Bacillus, Lysinibacillus genera [59].

Fish poisoning with scombrotoxin is the main cause of seafood poisoning. Studies by Bjornsdottir-Butler et al. [5, 6] assessed the number of histamine-producing bacteria in fish. One of the most common species of histamine-producing bacteria are R. planticola [5] and R. ornithinolytica [26]. Histamine-producing bacteria ussually have blaHDC gene. Sabry et al. [47] reported that hdc-positive strains exhibit higher levels of histamine that hdc-negative.

Besides toxins, bacteriocins are of importance in bac­terial pathogenicity of Raoultella spp. Fleming et al. [17] isolated from a strain of R. terrigena a substance with antimicrobial activity, which inhibited the growth of the following strains isolated from food samples E. coli, Klebsiella spp., Enterobacter spp. and Salmonella spp. The obtained bacteriocin was called raoultellin L, and it was proposed to be used as a biological weapon against food contaminating microorganisms. The ability to produce bacteriocins was also detected in R. ornithinolytica strains isolated from clinical specimens [44].

Additionally, Yu et al. [59] suggested that one of the essential virulence factors in Raoultella may be located at a pathogenicity island, similar to the reported in Yersinia spp. strains.

Further studies on Raoultella spp. morphology and biological properties are needed. Broadening the knowledge of and studying Raoultella spp. may help us to understand the pathomechanism of the infections they couse.

Use of Raoultella spp. in environmental protection

Taking into account the common occurrence of Raoultella strains in the natural environment, attention was paid to the possibility of using them for environment protection [7, 8, 34]. Sugimori et al. [53] used R. planticola 232-2 strain to decompose various fatty compounds, e.g. vegetable oil, beef tallow, oleic acid, lard. They proved that the degree of this degradation depends on the experimental conditions. The highest effectiveness was obtained at 35°C and pH 4.0. Further research needs to confirm whether the properties of Raoultella strains in the degradation of wastes derived from restaurants or sewage can be used in the future. Lipolytic activity of R. planticola and R. ornithinolytica strains was also confirmed by results from studies by Peil et al. [38]. They suggest the potential usefulness of these strains in different industry branches for biodegradation of lipidscontaining compounds.

Bidja-Abena et al. [4] isolated the R. ornithinolyitca PS strain, which decomposed to 83.5% of crude oil. This strain was more effective than Bacillus subtilis BJ11 (81.1%), Acinetobacter lwoffii BJ10 (75.8%), A. pittii BJ6 (74.9%) and Serratia marcescens PL (70.0%). All five strains degraded over 94% of crude oil after 10 days of incub­ation. In addition, these strains degraded straight alkanes, branched alkanes and aromatic hydrocarbons. The authors suggested the large potential of these strains in the remediation of an environment contamin­ated with crude oil.

The study by Alegbeleye et al. [1] showed that R. ornithinolytica degraded acenaphthene and fluorine (polycyclic aromatic hydrocarbon compounds). Among polycyclic aromatic hydrocarbon degrading bacteria R. ornithinolytica degraded fluorene most efficiently (99.90%). In turn, degradation of acenaphthene was 97.5% and R. ornith­inolytica was the second species, after Aeromonas hydrophila in term of degradation efficiency. Alegbeleye et al. [1] suggested that R. ornithinolytica can be used on a larger scale to restore polluted aquatic ecosystems.

De Lima Brossi et al. [11] described the enzymatic activity of R. terrigena strains. The studied strains have strong cellulolytic and xylanolytic activity, crucial for biopolymers degradation. In turn, Muňoz et al. [32] also investig­ated the ability of different strains to decompose paper. The authors have shown that R. ornithinolytica promotes cell wall degradation of microalgae through cellulolytic action at low temperatures, resulting in increased biogas production. Kim et al. [24] described R. ornithinolytica B6 strain that was able to use lignocellulose biomass for the production of 2,3-butanediol. R. ornithinolytica strains appeared to be the most effective in this field, which suggests the potential usefulness of these bacteria for paper decomposition.

The natural environment is contaminated by different toxic substances. In literature, there are available works about the degradation of trinitrotoluene by Raoultella spp. strains. The study by Thijs et al. [54] showed that 
R. ornithinolytica strain release nitrite from trinitrotoluene. The nitrite then can be used by plants for their growth. The analysed strain was isolated from forest soil at a military site in Belgium. In turn, Claus et al. [8] used the strain of R. terrigena for removing 2,4,6-trinitrotoluene from polluted environments, such as water. 2,4,6-trinitrotoluene is used for explosive material production. Its residues are toxic and mutagenic for the natural environment. The use of bacterial strains, e.g. R. terrigena, for degrading noxious substances may be useful in the protection of the natural environment [8, 34].

In turn, Skłodowska et al. [52] isolated the Raoutella strain, which reduced iron and precipitated uranium in sediments of the closed down uranium mine in Kowary (Poland). This strain was capable of dissim­ilatory reduction of iron (III) and uranium (VI) in the presence of citrate as an electron donor. The authors suggest that this may be useful in the bioremediation of uranium contaminated waters and sediments. The possibility of using Raoultella for disintegrating or mineralizing pollutants into less harmful or non-toxic compounds was also investigated by other authors [39, 58]. Ping et al. [40] described the high potential of 
R. planticola strain for bioremediation of the soil contaminated with aromatic polycyclic hydrocarbons.

Shin et al. [51] and Kim et al. [24] described the potential advantages of 2,3-butanediol production using R. ornithinolytica strains. The important characteristic of this strain is the possibility of using different saccharides as the only carbon source (glucose, fructose, galactose, galactose and xylose). 2,3-butanediol is an important substance for pesticides and drugs production. However, from the economic point of views, the common usage of these properties of bacterial strains in the massive scale industry is not possible.

Xu et al. [57] reported Raoultella spp. strain cadmium resistant. Cadmium is of the most concern in soils due to its high toxicity. The authors suggested that Raoultella spp. X13 strain is an effective treatment for potential application in cadmium remediation.

Production of antimicrobials by Raoultella spp.

The literature also includes works on the antimicrobial activity of Raoultella rods. Fiołka et al. [16] isolated from the Dendrobena veneta earthworm gut the R. ornithinolytica strain with antimicrobial activity against four species of fast-growing mycobacteria: Mycobacterium butiricum, M. jucho, M. smegmatis and M. phlei. Further research confirmed that the protein with a molecular mass above 100kDa is responsible for the anti-bacilli activity.

Also, Fiołka et al. [15] isolated the polysaccharide-protein complex, which is a metabolite of R. ornithinolytica with activity against Candida albicans fungi from the Dendrobena veneta earthworm gut. These authors noticed that the action of the complex disturbed metabolic activity and damaged the fungal cell wall. Researchers suggest the potential use of the complex as a fungicide component. These authors also observed the induction of tumour cell death by apoptosis and necrosis in the presence of the above complex. However, it was cytotoxic to human fibroblasts. Hence, there is a need for further research on its possible use in anti-cancer therapy.

Li et al. [28] discovered the nematicidal activity of R. terrigena against Meliodogyne incognito. It is a parasite of crops. Studies have confirmed that treating the cultivated plants with only R. terrigena suspension, and in combination with fresh wasabi extract, effectively combats Meliodogyne incognito on tomatoes.

In recent years, more studies have been published describing the virulence factors, diagnostics, biological properties and the possibility of using Raoultella strains in environmental protection, but some questions remain unanswered. Further studies will allow us to broaden the knowledge of Raoultella spp., explaining their virulence potential.

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