Pseudomonas
Pseudomonas is a genus of Gram-negative, Gammaproteobacteria, belonging to the family Pseudomonadaceae and containing 191 validly described species.[1] The members of the genus demonstrate a great deal of metabolic diversity and consequently are able to colonize a wide range of niches.[2] Their ease of culture in vitro and availability of an increasing number of Pseudomonas strain genome sequences has made the genus an excellent focus for scientific research; the best studied species include P. aeruginosa in its role as an opportunistic human pathogen, the plant pathogen P. syringae, the soil bacterium P. putida, and the plant growth-promoting P. fluorescens, P. lini, P. migulae, and P. graminis.[3][4]
Because of their widespread occurrence in water and plant seeds such as dicots, the pseudomonads were observed early in the history of microbiology. The generic name Pseudomonas created for these organisms was defined in rather vague terms by Walter Migula in 1894 and 1900 as a genus of Gram-negative, rod-shaped, and polar-flagellated bacteria with some sporulating species,[5][6] the latter statement was later proved incorrect and was due to refractive granules of reserve materials.[7] Despite the vague description, the type species, Pseudomonas pyocyanea (basonym of Pseudomonas aeruginosa), proved the best descriptor.[7]
Classification history
Like most bacterial genera, the pseudomonad[note 1] last common ancestor lived hundreds of millions of years ago. They were initially classified at the end of the 19th century when first identified by Walter Migula. The etymology of the name was not specified at the time and first appeared in the seventh edition of Bergey's Manual of Systematic Bacteriology (the main authority in bacterial nomenclature) as Greek pseudes (ψευδής) "false" and -monas (μονάς/μονάδος) "a single unit", which can mean false unit; however, Migula possibly intended it as false Monas, a nanoflagellated protist[7] (subsequently, the term "monad" was used in the early history of microbiology to denote unicellular organisms). Soon, other species matching Migula's somewhat vague original description were isolated from many natural niches and, at the time, many were assigned to the genus. However, many strains have since been reclassified, based on more recent methodology and use of approaches involving studies of conservative macromolecules.[8]
Recently, 16S rRNA sequence analysis has redefined the taxonomy of many bacterial species.[9] As a result, the genus Pseudomonas includes strains formerly classified in the genera Chryseomonas and Flavimonas.[10] Other strains previously classified in the genus Pseudomonas are now classified in the genera Burkholderia and Ralstonia.[11][12]
In 2020, a phylogenomic analysis of 494 complete Pseudomonas genomes identified two well-defined species (P. aeruginosa and P. chlororaphis) and four wider phylogenetic groups (P. fluorescens, P. stutzeri, P. syringae, P. putida) with a sufficient number of available proteomes.[13] The four wider evolutionary groups include more than one species, based on species definition by the Average Nucleotide Identity levels.[14] In addition, the phylogenomic analysis identified several strains that were mis-annotated to the wrong species or evolutionary group.[13] This mis-anotation problem has been reported by other analyses as well.[15]
Genomics
In 2000, the complete genome sequence of a Pseudomonas species was determined; more recently, the sequence of other strains has been determined, including P. aeruginosa strains PAO1 (2000), P. putida KT2440 (2002), P. protegens Pf-5 (2005), P. syringae pathovar tomato DC3000 (2003), P. syringae pathovar syringae B728a (2005), P. syringae pathovar phaseolica 1448A (2005), P. fluorescens Pf0-1, and P. entomophila L48.[8]
By 2016, more than 400 strains of Pseudomonas had been sequenced.[16] Sequencing the genomes of hundreds of strains revealed highly divergent species within the genus. In fact, many genomes of Pseudomonas share only 50-60% of their genes, e.g. P. aeruginosa and P. putida share only 2971 proteins out of 5350 (or ~55%).[16]
By 2020, more than 500 complete Pseudomonas genomes were available in Genebank. A phylogenomic analysis utilized 494 complete proteomes and identified 297 core orthologues, shared by all strains.[13] This set of core orthologues at the genus level was enriched for proteins involved in metabolism, translation, and transcription and was utilized for generating a phylogenomic tree of the entire genus, to delineate the relationships among the Pseudomonas major evolutionary groups.[13] In addition, group-specific core proteins were identified for most evolutionary groups, meaning that they were present in all members of the specific group, but absent in other Pseudomonads. For example, several P. aeruginosa-specific core proteins were identified that are known to play an important role in this species' pathogenicity, such as CntL, CntM, PlcB, Acp1, MucE, SrfA, Tse1, Tsi2, Tse3, and EsrC.[13]
Characteristics
Members of the genus display these defining characteristics:[17]
- Rod-shaped
- Gram-negative
- Flagellum one or more, providing motility
- Aerobic
- Non-spore forming
- Catalase-positive
- Oxidase-positive
Other characteristics that tend to be associated with Pseudomonas species (with some exceptions) include secretion of pyoverdine, a fluorescent yellow-green siderophore[18] under iron-limiting conditions. Certain Pseudomonas species may also produce additional types of siderophore, such as pyocyanin by Pseudomonas aeruginosa[19] and thioquinolobactin by Pseudomonas fluorescens,.[20] Pseudomonas species also typically give a positive result to the oxidase test, the absence of gas formation from glucose, glucose is oxidised in oxidation/fermentation test using Hugh and Leifson O/F test, beta hemolytic (on blood agar), indole negative, methyl red negative, Voges–Proskauer test negative, and citrate positive.
Pseudomonas may be the most common nucleator of ice crystals in clouds, thereby being of utmost importance to the formation of snow and rain around the world.[21]
Biofilm formation
All species and strains of Pseudomonas have historically been classified as strict aerobes. Exceptions to this classification have recently been discovered in Pseudomonas biofilms.[22] A significant number of cells can produce exopolysaccharides associated with biofilm formation. Secretion of exopolysaccharides such as alginate makes it difficult for pseudomonads to be phagocytosed by mammalian white blood cells.[23] Exopolysaccharide production also contributes to surface-colonising biofilms that are difficult to remove from food preparation surfaces. Growth of pseudomonads on spoiling foods can generate a "fruity" odor.
Antibiotic resistance
Most Pseudomonas spp. are naturally resistant to penicillin and the majority of related beta-lactam antibiotics, but a number are sensitive to piperacillin, imipenem, ticarcillin, or ciprofloxacin.[23] Aminoglycosides such as tobramycin, gentamicin, and amikacin are other choices for therapy.
This ability to thrive in harsh conditions is a result of their hardy cell walls that contain porins. Their resistance to most antibiotics is attributed to efflux pumps, which pump out some antibiotics before they are able to act.
Pseudomonas aeruginosa is increasingly recognized as an emerging opportunistic pathogen of clinical relevance. One of its most worrying characteristics is its low antibiotic susceptibility.[24] This low susceptibility is attributable to a concerted action of multidrug efflux pumps with chromosomally encoded antibiotic resistance genes (e.g., mexAB-oprM, mexXY, etc.,[25]) and the low permeability of the bacterial cellular envelopes. Besides intrinsic resistance, P. aeruginosa easily develops acquired resistance either by mutation in chromosomally encoded genes or by the horizontal gene transfer of antibiotic resistance determinants. Development of multidrug resistance by P. aeruginosa isolates requires several different genetic events that include acquisition of different mutations and/or horizontal transfer of antibiotic resistance genes. Hypermutation favours the selection of mutation-driven antibiotic resistance in P. aeruginosa strains producing chronic infections, whereas the clustering of several different antibiotic resistance genes in integrons favours the concerted acquisition of antibiotic resistance determinants. Some recent studies have shown phenotypic resistance associated to biofilm formation or to the emergence of small-colony-variants, which may be important in the response of P. aeruginosa populations to antibiotic treatment.[8]
Sensitivity to gallium
Although gallium has no natural function in biology, gallium ions interact with cellular processes in a manner similar to iron(III). When gallium ions are mistakenly taken up in place of iron(III) by bacteria such as Pseudomonas, the ions interfere with respiration, and the bacteria die. This happens because iron is redox-active, allowing the transfer of electrons during respiration, while gallium is redox-inactive.[26][27]
Pathogenicity
Animal pathogens
Infectious species include P. aeruginosa, P. oryzihabitans, and P. plecoglossicida. P. aeruginosa flourishes in hospital environments, and is a particular problem in this environment, since it is the second-most common infection in hospitalized patients (nosocomial infections)[citation needed]. This pathogenesis may in part be due to the proteins secreted by P. aeruginosa. The bacterium possesses a wide range of secretion systems, which export numerous proteins relevant to the pathogenesis of clinical strains.[28] Intriguingly, several genes involved in the pathogenesis of P.aeruginosa, such as CntL, CntM, PlcB, Acp1, MucE, SrfA, Tse1, Tsi2, Tse3, and EsrC are core group-specific,[13] meaning that they are shared by the vast majority of P. aeruginosa strains, but they are not present in other Pseudomonads.
Plant pathogens
P. syringae is a prolific plant pathogen. It exists as over 50 different pathovars, many of which demonstrate a high degree of host-plant specificity. Numerous other Pseudomonas species can act as plant pathogens, notably all of the other members of the P. syringae subgroup, but P. syringae is the most widespread and best-studied.
Although not strictly a plant pathogen, P. tolaasii can be a major agricultural problem, as it can cause bacterial blotch of cultivated mushrooms.[29] Similarly, P. agarici can cause drippy gill in cultivated mushrooms.[30]
Use as biocontrol agents
Since the mid-1980s, certain members of the genus Pseudomonas have been applied to cereal seeds or applied directly to soils as a way of preventing the growth or establishment of crop pathogens. This practice is generically referred to as biocontrol. The biocontrol properties of P. fluorescens and P. protegens strains (CHA0 or Pf-5 for example) are currently best-understood, although it is not clear exactly how the plant growth-promoting properties of P. fluorescens are achieved. Theories include: the bacteria might induce systemic resistance in the host plant, so it can better resist attack by a true pathogen; the bacteria might outcompete other (pathogenic) soil microbes, e.g. by siderophores giving a competitive advantage at scavenging for iron; the bacteria might produce compounds antagonistic to other soil microbes, such as phenazine-type antibiotics or hydrogen cyanide. Experimental evidence supports all of these theories.[31]
Other notable Pseudomonas species with biocontrol properties include P. chlororaphis, which produces a phenazine-type antibiotic active agent against certain fungal plant pathogens,[32] and the closely related species P. aurantiaca, which produces di-2,4-diacetylfluoroglucylmethane, a compound antibiotically active against Gram-positive organisms.[33]
Use as bioremediation agents
Some members of the genus are able to metabolise chemical pollutants in the environment, and as a result, can be used for bioremediation. Notable species demonstrated as suitable for use as bioremediation agents include:
- P. alcaligenes, which can degrade polycyclic aromatic hydrocarbons.[34]
- P. mendocina, which is able to degrade toluene.[35]
- P. pseudoalcaligenes, which is able to use cyanide as a nitrogen source.[36]
- P. resinovorans, which can degrade carbazole.[37]
- P. veronii, which has been shown to degrade a variety of simple aromatic organic compounds.[38][39]
- P. putida, which has the ability to degrade organic solvents such as toluene.[40] At least one strain of this bacterium is able to convert morphine in aqueous solution into the stronger and somewhat expensive to manufacture drug hydromorphone (Dilaudid).
- Strain KC of P. stutzeri, which is able to degrade carbon tetrachloride.[41]
Detection of food spoilage agents in milk
One way of identifying and categorizing multiple bacterial organisms in a sample is to use ribotyping.[42] In ribotyping, differing lengths of chromosomal DNA are isolated from samples containing bacterial species, and digested into fragments.[42] Similar types of fragments from differing organisms are visualized and their lengths compared to each other by Southern blotting or by the much faster method of polymerase chain reaction (PCR).[42] Fragments can then be matched with sequences found on bacterial species.[42] Ribotyping is shown to be a method to isolate bacteria capable of spoilage.[43] Around 51% of Pseudomonas bacteria found in dairy processing plants are P. fluorescens, with 69% of these isolates possessing proteases, lipases, and lecithinases which contribute to degradation of milk components and subsequent spoilage.[43] Other Pseudomonas species can possess any one of the proteases, lipases, or lecithinases, or none at all.[43] Similar enzymatic activity is performed by Pseudomonas of the same ribotype, with each ribotype showing various degrees of milk spoilage and effects on flavour.[43] The number of bacteria affects the intensity of spoilage, with non-enzymatic Pseudomonas species contributing to spoilage in high number.[43]
Food spoilage is detrimental to the food industry due to production of volatile compounds from organisms metabolizing the various nutrients found in the food product.[44] Contamination results in health hazards from toxic compound production as well as unpleasant odours and flavours.[44] Electronic nose technology allows fast and continuous measurement of microbial food spoilage by sensing odours produced by these volatile compounds.[44] Electronic nose technology can thus be applied to detect traces of Pseudomonas milk spoilage and isolate the responsible Pseudomonas species.[45] The gas sensor consists of a nose portion made of 14 modifiable polymer sensors that can detect specific milk degradation products produced by microorganisms.[45] Sensor data is produced by changes in electric resistance of the 14 polymers when in contact with its target compound, while four sensor parameters can be adjusted to further specify the response.[45] The responses can then be pre-processed by a neural network which can then differentiate between milk spoilage microorganisms such as P. fluorescens and P. aureofaciens.[45]
Species previously classified in the genus
Recently, 16S rRNA sequence analysis redefined the taxonomy of many bacterial species previously classified as being in the genus Pseudomonas.[9] Species removed from Pseudomonas are listed below; clicking on a species will show its new classification. The term 'pseudomonad' does not apply strictly to just the genus Pseudomonas, and can be used to also include previous members such as the genera Burkholderia and Ralstonia.
α proteobacteria: P. abikonensis, P. aminovorans, P. azotocolligans, P. carboxydohydrogena, P. carboxidovorans, P. compransoris, P. diminuta, P. echinoides, P. extorquens, P. lindneri, P. mesophilica, P. paucimobilis, P. radiora, P. rhodos, P. riboflavina, P. rosea, P. vesicularis.
β proteobacteria: P. acidovorans, P. alliicola, P. antimicrobica, P. avenae, P. butanovorae, P. caryophylli, P. cattleyae, P. cepacia, P. cocovenenans, P. delafieldii, P. facilis, P. flava, P. gladioli, P. glathei, P. glumae, P. graminis, P. huttiensis, P. indigofera, P. lanceolata, P. lemoignei, P. mallei, P. mephitica, P. mixta, P. palleronii, P. phenazinium, P. pickettii, P. plantarii, P. pseudoflava, P. pseudomallei, P. pyrrocinia, P. rubrilineans, P. rubrisubalbicans, P. saccharophila, P. solanacearum, P. spinosa, P. syzygii, P. taeniospiralis, P. terrigena, P. testosteroni.
γ-β proteobacteria: P. beteli, P. boreopolis, P. cissicola, P. geniculata, P. hibiscicola, P. maltophilia, P. pictorum.
γ proteobacteria: P. beijerinckii, P. diminuta, P. doudoroffii, P. elongata, P. flectens, P. halodurans, P. halophila, P. iners, P. marina, P. nautica, P. nigrifaciens, P. pavonacea,[46] P. piscicida, P. stanieri.
δ proteobacteria: P. formicans.
Bacteriophage
There are a number of bacteriophages that infect Pseudomonas, e.g.
- Pseudomonas phage Φ6
- Pseudomonas aeruginosa phage EL [47]
- Pseudomonas aeruginosa phage ΦKMV [48]
- Pseudomonas aeruginosa phage LKD16 [49]
- Pseudomonas aeruginosa phage LKA1 [49]
- Pseudomonas aeruginosa phage LUZ19
- Pseudomonas aeruginosa phage ΦKZ [47]
- Pseudomonas putida phage gh-1 [50]
See also
- Culture collection for a list of culture collections
Footnotes
- ^ To aid in the flow of the prose in English, genus names can be "trivialised" to form a vernacular name to refer to a member of the genus: for the genus Pseudomonas it is "pseudomonad" (plural: "pseudomonads"), a variant on the non-nominative cases in the Greek declension of monas, monada.[51] For historical reasons, members of several genera that were formerly classified as Pseudomonas species can be referred to as pseudomonads, while the term "fluorescent pseudomonad" refers strictly to current members of the genus Pseudomonas, as these produce pyoverdin, a fluorescent siderophore.[2] The latter term, fluorescent pseudomonad, is distinct from the term P. fluorescens group, which is used to distinguish a subset of members of the Pseudomonas sensu stricto and not as a whole
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