Enterobacter

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Enterobacter
Enterobacter cloacae Colonies of different appearance on a nutrient agar plate

Enterobacter cloacae
Colonies of different appearance on a nutrient agar plate

Systematics
Domain : Bacteria (bacteria)
Department : Proteobacteria
Class : Gammaproteobacteria
Order : Enterobacteria (Enterobacterales)
Family : Enterobacteriaceae
Genre : Enterobacter
Scientific name
Enterobacter
Hormaeche & Edwards 1960
emend. Brady et al. 2013

Enterobacter is a genus of bacteria belonging to the family of the Enterobacteriaceae belongs and about 15 species comprises. Representatives of the Enterobacter genusare found in almost all habitats, including the human intestine . There they belong to the normal intestinal flora . The rod-shaped bacterial cells arestained redin the Gram stain and therefore belong to the group of Gram- negative bacteria. They are able toactively movewith the help of flagella . They can live with or without oxygen and are therefore referred to as facultative anaerobic life forms. If there is no oxygen, they lead to energy a fermentation by. Thefermentation typicalfor Enterobacter is the 2,3-butanediol fermentation - this is an important distinguishing feature from related genera.

General statements on the pathogenicity of Enterobacter as a pathogen are difficult: There are species that are not considered pathogenic, but also species that can cause disease in humans (classification in risk group  2 according to the Biological Agents Ordinance ). It used to be assumed that representatives of the genus are at best to be seen as opportunistic pathogens that can cause infectious diseases in patients with an already weakened immune system . The antibiotic resistance of some Enterobacter species (especially Enterobacter cloacae ), which has been observed for a few decades , means that they are now of increasing importance as pathogens for infections acquired in hospital - nosocomial infections . In addition, it is noteworthy that the systematics of the genus or related genera is constantly changing due to phylogenetic studies of various genes . This has led to the fact that some types of bacteria are no longer assigned to the Enterobacter genus , but to other genera, some of which have been newly described. For example, Enterobacter agglomerans , which occurs in some plants, has belonged to its own genus Pantoea since 1989 and the medically relevant species Enterobacter aerogenes and Enterobacter sakazakii are now known as Klebsiella aerogenes and Cronobacter sakazakii , respectively .

features

Appearance

The cells of Enterobacter species are rod-shaped and actively mobile ( motile ) through flagella ; the latter distinguishes them from the related genus Klebsiella . The flagella (also called flagella) are arranged peritrich . A single cell is approximately 0.5 µm wide and 2-3 µm long. In Gram staining , the cells behave gram- negative, i.e. they are stained pink to red by the dyes used. There are no persistence forms such as endospores .

In Enterobacter cloacae , the bacterial cell wall is surrounded by a capsule made of polysaccharides . They are involved in the formation of biofilms and give the bacterial colonies that have grown on a nutrient medium a slimy appearance. Sometimes there are cells that lack the capsule, the colonies that have grown look rather rough, this can be seen in the picture above. Other Enterobacter species also form a capsule, but there is no uniform picture within the genus. Representatives of the Enterobacter genus show good growth on common nutrient media. Their colonies are usually not particularly colored, in contrast to the yellowish colored colonies of Cronobacter sakazakii .

Growth and metabolism

The members of the genus Enterobacter are chemoorganotroph , i. In other words, they break down organic substances to generate energy . They are facultatively anaerobic : If oxygen is present, they can carry out an oxidative energy metabolism , they oxidize the organic substances to carbon dioxide (CO 2 ) and water; if no oxygen is available, i.e. under anoxic conditions, they use 2,3-butanediol fermentation to generate energy. The end products here are mainly the alcohol 2,3-butanediol and CO 2 in large quantities , and also in small quantities and the like. a. different acids. In other genera of the Enterobacteriaceae family such. B. Escherichia and Salmonella , mixed acid fermentation is the anaerobic energy metabolic pathway, whereby, in contrast to butanediol fermentation , large amounts of acids ( acetic acid , lactic acid and succinic acid ) are produced as end products, but no butanediol. This characteristic is used to differentiate the enterobacteria genera (see section Evidence ). As is typical for Enterobacteriaceae, the catalase test is positive and the oxidase test is negative.

Simple nutrient media are suitable for cultivation ; no special growth factors are necessary. The bacteria can be grown, for example, on casein soy peptone agar (CASO agar), blood agar is also suitable, as is selective nutrient media that are suitable for isolating and differentiating between representatives of enterobacteria, for example MacConkey agar or eosin methylene blue - Agar (EMB). Enterobacter species are mesophilic , optimal growth occurs in a temperature range of 30 to 37 ° C, colonies with a diameter of 2-3 mm are already visible after one day of incubation . Some types, e.g. B. E. cloacae also grow at lower temperatures (15-25 ° C), for example in the brackish water of coastal regions with a temperate climate.

Chemotaxonomy

The GC content , ie the proportion of the nucleobases guanine and cytosine in the bacterial DNA , is 52–60  mol percent . Components of the bacterial cell act as antigens , the somatic O-antigens and the H-antigens are of diagnostic importance (compare the Kauffmann-White scheme used for Salmonella ).

Pathogenicity

General statements on the pathogenicity of Enterobacter are difficult because the systematics of the genus and related genera is constantly changing. Furthermore, in older reports there is often a mix-up or no clear distinction between Enterobacter and Klebsiella . Species that were considered medically relevant in the past no longer belong to the genus (the well-known examples E. aerogenes and E. sakazakii ). In the specialist literature, common statements are often made for E. cloacae and E. aerogenes , so that when the last-named bacterial species is transferred to the genus Klebsiella (2017), a clear assignment of statements on pathogenicity is problematic.

In the middle of the 20th century, Enterobacter species were rarely described as pathogenic, but this changed with the increasing consumption of antibiotics . Meanwhile, several representatives of the genus play a role in nosocomial infections ("hospital infections "), especially since they are resistant to some antibiotics. Infections that occur in hospitals are particularly vulnerable to immunosuppressed patients; urinary tract infections and bacteremia have been reported in this context . E. cancerogenus ( E. taylorae ) was named as the pathogen in 1987 in a case of osteomyelitis , an infectious inflammation of the bone marrow.

E. asburiae , E. bugandensis , E. cancerogenus , E. hormaechei , E. Kobei , E. ludwigii and E. cloacae subsp. cloacae are  assigned to risk group 2 by the Biological Agents Ordinance in conjunction with the TRBA ( Technical Rules for Biological Agents) 466 . The species E. mori , E. muelleri , E. siamensis , E. soli , E. tabaci , E. xiangfangensis and E. cloacae subsp. dissolvens belong to risk group 1 (they are regarded as non-pathogenic).

proof

Enterobacter cloacae in the Voges-Proskauer test with positive result

There is no special nutrient medium that is selective for Enterobacter species for isolating bacteria from environmental samples or clinical material . Instead, selective nutrient media for enterobacteria are used, with the following further identification.

Biochemical evidence

Biochemical features, such as the enzymes present and the resulting metabolic properties, can be used in a colored row to identify Enterobacter species or to distinguish them from other representatives of the Enterobacteriaceae. Typically, the Voges-Proskauer test is used. The test detects acetoin , an intermediate product of 2,3-butanediol fermentation. Enterobacter and Klebsiella react positively, Escherichia, however, negatively. Other reactions in the so-called IMViC test procedure also serve to distinguish between Escherichia and Enterobacter :

Table: IMViC reactions of Escherichia coli and Enterobacter cloacae
Microorganism Indole formation Methyl red sample Acetoin formation Citrate utilization
Escherichia coli + + - -
Enterobacter cloacae - - + +

Representatives of the Enterobacter genus utilize the carbohydrates glucose and lactose in a fermentation with the formation of gas and acid. The fermentation of glucose produces a lot of carbon dioxide (CO 2 ), at least twice as much as hydrogen (H 2 ). In the case of individual bacterial strains , there is no uniform picture with regard to lactose utilization. For some species, therefore, the statement "variable" is used, ie. that is, there are both strains that can break down lactose and strains that cannot. In the case of selective nutrient media, the detection of lactose degradation is often carried out via the acid formation during fermentative degradation of the carbohydrate; the pH indicator contained in the nutrient medium changes its color through the acid formation . Some strains may show a negative or only weakly positive result because too little acid is produced. On the other hand, the ONPG test is positive, even if the lactose detection due to acid formation was negative after 48 hours of incubation. This biochemical evidence shows that the bacteria have the enzyme β-galactosidase at their disposal, with which lactose is hydrolyzed into the two components glucose and galactose .

Other carbohydrates that many members of the genus can use include, for example, the monosaccharides L - arabinose , L - rhamnose and D - xylose , the disaccharide D - cellobiose , the trisaccharide raffinose and the sugar alcohol D - mannitol . There is no formation of hydrogen sulfide (H 2 S), on the other hand the splitting of aesculin proceeds positively and aesculin is hydrolyzed. The enzyme urease is not present, so urea cannot be broken down. Although E. gergoviae is urease-positive, it is no longer included in the genus (see section Systematics ). With regard to other enzymes that are tested in biochemical test systems, ornithine decarboxylase (ODC) is present - an important criterion for differentiating the ODC-negative Klebsiellae - while the enzymes lysine decarboxylase (LDC) and arginine dihydrolase (ADH) only occur in some species can thus be used to differentiate between them.

A standardized and miniaturized test system for rapid identification, inoculated with Enterobacter cloacae , incubated for 1 day

In order to identify the individual Enterobacter species, biochemical tests that are based on the breakdown of various organic compounds and indicate the metabolic products formed are suitable; miniaturized test systems can be used for this. The compounds useful for this are, for example, L - fucose , D - lyxose , D - maltitol , D - melibiose , sucrose and D - sorbitol .

Further evidence

A serological differentiation between different strains of E. cloacae is possible. In this case, be antibodies against the 53 somatic O antigens and 56 established by the flagellar H antigens used. Almost 80 different serotypes can be distinguished. However, the procedure is not yet used in epidemiological investigations.

Molecular biological methods are well suited for differentiating and thus for identifying different Enterobacter species. The detection of certain parts of the bacterial genome with the aid of the PCR method ( polymerase chain reaction ) is specific . In this process, gene segments that are typical for the type of bacteria are duplicated ( amplified ) and detected. A process developed in 2012 is based on the Real Time Quantitative PCR ( q-PCR ) from an as dnaJ designated nucleotide sequence . For this purpose, the bacteria are first cultivated on the selective nutrient medium Endo-Agar and then their DNA is extracted . A primer pair that matches the gene segment enables the amplification and quantitative determination of the gene segments present and thus identification of the bacterium. The method developed in Germany aims to detect E. cloacae , which is differentiated from the other species of the so-called E. cloacae complex (consisting of E. asburiae , E. cloacae , E. hormaechei , E. kobei , E. ludwigii and E. nimipressuralis ) can be distinguished. Further modifications of the PCR method are also used for identification, for example with randomly amplified polymorphic DNA ( RAPD ), its variant AP-PCR (arbitrary primed PCR, PCR with arbitrarily - arbitrarily - chosen primers) or the repetitive sequence-based PCR (rep-PCR ). An investigation method based on molecular biological methods is pulsed field gel electrophoresis (PFGE), which is used in the case of epidemic outbreaks in newborn intensive care units to clarify the pathogens involved. PFGE is also used to identify Cronobacter spp. used.

The identification with the help of the MALDI-TOF method in combination with mass spectrometry (MS) is suitable for detecting Enterobacter , but the differentiation between closely related species (so-called E. cloacae complex) is not reliable. Another investigation shows that although it is possible to differentiate between E. cloacae complex and E. aerogenes (now Klebsiella aerogenes ) using MALDI-TOF MS, the differentiation within the complex is not clear.

Systematics and taxonomy

Descriptions of bacteria that can be traced back to Enterobacter species have existed since the end of the 19th century (“ Bacillus cloacae ” Jordan 1890). Synonyms for Enterobacter are " Cloaca " Castellani & Chalmers 1919 and " Aerobacter " Hormaeche & Edwards 1958, but these names are no longer valid. The genus Enterobacter is not the type genus of the Enterobacteriaceae family, this is the genus Escherichia . This deviates from Rule 21a in conjunction with Rule 9 of the nomenclature according to the Bacteriological Code ( International Code of Nomenclature of Bacteria ), which was established in 1958 in Judicial Opinion 15 of the Judicial Commission (for example, “judicial or impartial commission”) of the International Commission for the Systematics of Prokaryotes ( International Committee on Systematics of Prokaryotes , ICSP) was established. Type species of the genus is Enterobacter cloacae ( Jordan 1890) Hormaeche & Edwards 1960.

External system

The genus Enterobacter belongs to the Enterobacteriaceae family in the order Enterobacterales Adeolu et al. 2016, which belongs to the class of Gammaproteobacteria . The Enterobacterales order established in 2016 includes eight families with a total of around 60 genera. The newly established and thus the rules of the bacteriological code (ICBN) corresponding type genus of the order Enterobacterales Adeolu et al. 2016 is the genus Enterobacter . The Enterobacteriaceae form a large group of gram-negative bacteria to which u. a. the genera Citrobacter , Escherichia , Klebsiella , Raoultella , Salmonella and Shigella belong, some of which are important as pathogens .

The work of Hormaeche and Edwards from 1960 was based on the problem that in the genus called “ Aerobacter ” (with the then recognized species “ Aerobacter aerogenes ” and “ Aerobacter cloacae ”) both motile and non-motile bacteria were classified, whereby the latter would be assigned to the genus Klebsiella , which was already proven by serological and biochemical tests at that time. The new name as Enterobacter instead of “ Aerobacter ” and the description of the typical characteristics should help to enable scientists working in the field to clearly classify newly described species. One consequence of this is the reclassification of Enterobacter aerogenes as Klebsiella aerogenes in 2017 . It had already been recognized in 1971 that E. aerogenes and K. mobilis are homotypic synonyms , since both species have the same type strain. It has also been discussed in the past that Enterobacter belong to the Klebsielleae tribe due to phenotypic similarities with Klebsiella and other genera . The tribal rank is no longer common since the revision (1990) of the International Code of Nomenclature of Bacteria (Bacteriological Code).

Further investigations showed that different species of Erwinia phenotypically resembled species of the Enterobacter genus , which is why they were placed in this genus, e.g. Erwinia herbicola as Enterobacter agglomerans , but which has belonged to a separate genus Pantoea since 1989 . Mainly through genetic studies, e.g. B. DNA-DNA hybridization and multi- locus sequence analysis ( MLSA , here only certain genes are examined) changed the systematics of enterobacteria fundamentally. Numerous Enterobacter species have been found to belong to other, newly described genera. The work of Brady et al. 2013 led to the first description of Kosakonia , Lelliottia and Pluralibacter , as well as an extended description of the genera Cronobacter and Enterobacter .

Internal system

Investigations in the period from 2004 to 2005 of Enterobacter dissolvens showed that it is a subspecies (subspecies) of E. cloacae . During the same period, three medically relevant subspecies of E. hormaechei were described, but they were only validly published in 2016. Because of the difficult distinction between closely related species, the term E. cloacae complex is used in medical microbiology , consisting of E. asburiae , E. cloacae , E. hormaechei , E. kobei , E. ludwigii and E. nimipressuralis . Other authors include E. asburiae , E. cancerogenus , E. cloacae and E. ludwigii .

Currently (as of December 2019) the genus includes the following species and subspecies, E. cloacae is the type species. In addition, the list also includes bacteria that previously belonged to the Enterobacter genus , but have now been assigned to other genera; this is indicated by an arrow behind the name with a reference to the current designation.

  • Enterobacter aerogenes Hormaeche & Edwards 1960 (Synonym Klebsiella mobilis Bascomb et al. 1971) → Klebsiella aerogenes ( Hormaeche & Edwards 1960) Tindall et al. 2017, comb. nov.
  • Enterobacter agglomerans Ewing & Fife 1972 → Pantoea agglomerans ( Ewing & Fife 1972) Gavini et al. 1989, comb. nov.
  • Enterobacter amnigenus Izard et al. 1981 → Lelliottia amnigena ( Izard et al. 1981) Brady et al. 2013, comb. nov.
  • Enterobacter arachidis Madhaiyan et al. 2010 → Kosakonia arachidis ( Madhaiyan et al. 2010) Brady et al. 2013, comb. nov.
  • Enterobacter asburiae Brenner et al. 1988 emend. Hoffmann et al. 2005, previously referred to as “CDC Enteric group 17”
  • Enterobacter bugandensis Doijad et al. 2016, sp. nov.
  • Enterobacter cancerogenus ( Urosevic 1966) Dickey & Zumoff 1988, comb. nov. (Synonym Erwinia cancerogena Urosevic 1966 (Approved Lists 1980)), previously referred to as “CDC Enteric group 19”
  • Enterobacter cloacae ( Jordan 1890) Hormaeche & Edwards 1960
  • Enterobacter cloacae subsp. cloacae ( Jordan 1890) Hoffmann et al. 2005 subsp. nov.
  • Enterobacter cloacae subsp. dissolvens ( Rosen 1922) Hoffmann et al. 2005 subsp. nov.
  • Enterobacter cowanii Inoue et al. 2001 → Kosakonia cowanii ( Inoue et al. 2001) Brady et al. 2013, comb. nov.
  • Enterobacter dissolvens ( Rosen 1922) Brenner et al. 1988 → E. cloacae subsp. dissolvens ( Rosen 1922) Hoffmann et al. 2005 subsp. nov.
  • Enterobacter gergoviae Brenner et al. 1980 → Pluralibacter gergoviae ( Brenner et al. 1980) Brady et al. 2013, comb. nov.
  • Enterobacter helveticus Stephan et al. 2007 → Cronobacter helveticus ( Stephan et al. 2007) Brady et al. 2013, comb. nov.
  • Enterobacter hormaechei O'Hara et al. 1990 emend. Hoffmann et al. 2016, previously referred to as “CDC Enteric group 75”
  • Enterobacter hormaechei subsp. hormaechei Hoffmann et al. 2016 subsp. nov.
  • Enterobacter hormaechei subsp. oharae Hoffmann et al. 2016 subsp. nov.
  • Enterobacter hormaechei subsp. steigerwaltii Hoffmann et al. 2016 subsp. nov.
  • Enterobacter intermedius corrig. Izard et al. 1980, sp. nov. → Kluyvera intermedia ( Izard et al. 1980) Pavan et al. 2005, comb. nov.
  • Enterobacter kobei Kosako et al. 1988 emend. Hoffmann et al. 2005, previously referred to as “NIH group 21”
  • Enterobacter ludwigii Hoffmann et al. 2005 sp. nov.
  • Enterobacter massiliensis Lagier et al. 2014 sp. nov. → Metakosakonia massiliensis ( Lagier et al. 2014) Alnajar & Gupta 2017, comb. nov.
  • Enterobacter mori Zhu et al. 2011 sp. nov.
  • Enterobacter muelleri KAMPER et al. 2015 sp. nov.
  • Enterobacter nimipressuralis ( Carter 1945) Brenner et al. 1988, comb. nov. → Lelliottia nimipressuralis ( Carter 1945) Brady et al. 2013, comb. nov.
  • Enterobacter oryzae Peng et al. 2009, sp. nov. → Kosakonia oryzae ( Peng et al. 2009) Brady et al. 2013, comb. nov.
  • Enterobacter oryzendophyticus Hardoim et al. 2015, sp. nov. → Kosakonia oryzendophytica ( Hardoim et al. 2015) Li et al. 2016, comb. nov.
  • Enterobacter oryziphilus Hardoim et al. 2015, sp. nov. → Kosakonia oryziphila ( Hardoim et al. 2015) Li et al. 2016, comb. nov.
  • Enterobacter pulveris Stephan et al. 2008, sp. nov. → Cronobacter pulveris ( Stephan et al. 2008) Brady et al. 2013, comb. nov.
  • Enterobacter pyrinus Chung et al. 1993, sp. nov. → Pluralibacter pyrinus ( Chung et al. 1993) Brady et al. 2013, comb. nov.
  • Enterobacter radicincitans fighter et al. 2005, sp. nov. → Kosakonia radicincitans ( fighters et al. 2005) Brady et al. 2013, comb. nov.
  • Enterobacter sacchari Zhu et al. 2013, sp. nov. → Kosakonia sacchari ( Zhu et al. 2013) Gu et al. 2014, comb. nov.
  • Enterobacter sakazakii Farmer et al. 1980, sp. nov. → Cronobacter sakazakii ( Farmer et al. 1980) Iversen et al. 2008, comb. nov.
  • Enterobacter siamensis Khunthongpan et al. 2014, sp. nov.
  • Enterobacter soli Manter et al. 2011, sp. nov.
  • Enterobacter tabaci Duan et al. 2016, sp. nov.
  • Enterobacter taylorae Farmer et al. 1985, sp. nov. → E. cancerogenus ( Urosevic 1966) Dickey & Zumoff 1988, comb. nov.
  • Enterobacter turicensis Stephan et al. 2007, sp. nov. → Cronobacter zurichensis ( Stephan et al. 2007) Brady et al. 2013, nom. nov.
  • Enterobacter xiangfangensis Gu et al. 2014, sp. nov.

Etymology and Eponyms

The name Enterobacter is derived from enteron ( ancient Greek ἕντερον 'intestine') and the Latinized word bacter for ancient Greek βακτηρΐα 'stick', consequently means something like "small rod bacterium in the intestine". The idea for this name comes from the German-Danish bacteriologist Fritz Kauffmann .

For numerous Enterobacter species, the scientists who first described them selected an epithet that represents an eponym , i.e. a word derived from a proper name. E. hormaechei was named in honor of Estenio Hormaeche (Uruguayan microbiologist), he defined the genus together with Philip R. Edwards. The epithet of E. ludwigii is dedicated to the German microbiologist Wolfgang Ludwig , who contributed to the understanding of the bacteria system. Mary Alyce Fife-Asbury (US microbiologist), Hans Emil Müller (German microbiologist) and Welton Taylor (US microbiologist) “were the godfathers” for E. asburiae , E. muelleri and E. taylorae , which three scientists have basic knowledge about the Enterobacteriaceae obtained and published.

But the people who honored their colleagues by using an eponym were also mentioned in reverse by other scientists in an epithet of a subspecies: Caroline M. O'Hara and Arnold G. Steigerwalt, both American microbiologists, the E. hormaechei first described can be found in E. hormaechei subsp. oharae and E. hormaechei subsp. steigerwaltii again.

Occurrence

In their article A proposed genus Enterobacter from 1960, Hormaeche and Edwards describe the occurrence of the two Enterobacter species known at the time as “ widely distributed in nature. “(German: 'Widespread in nature.'). Even decades later, this statement is still true, however, when specifying the ecology of Enterobacter , it should be taken into account how often the systematics of the genus or related genera has changed. For example, a bacterium associated with plants was first designated as Erwinia herbicola , then as Enterobacter agglomerans and now as Pantoea agglomerans .

Natural habitats of the representatives of the genus are bodies of water , sewage , brackish water , plants and soil . Several types are also found on the skin and intestines of humans and animals , in meat , raw milk and in hospitals . In animal stalls they occur as bioaerosols in the order of magnitude of up to 10 4 colony-forming units per cubic meter of air. If found in food, contamination in the manufacturing process is to be assumed; this applies, for example, to milk products such as yoghurt and cheese and can also be the case with powdered infant formula . In medical samples such as urine , faeces , blood , sputum and wounds , E. asburiae , E. cancerogenus , E. cloacae subsp. cloacae and E. hormaechei detected. In contrast, Enterobacter cloacae subsp. dissolvens was only found in environmental samples; it was first isolated from rotting stalks in 1922. E. soli was isolated from soil in 2011 and is able to break down lignin .

Some of the members of the genus discovered in recent years ( E. bugandensis , E. kobei , E. ludwigii and E. massiliensis ) were discovered in medical test material, although these are not necessarily pathogens. E. massiliensis was isolated as part of a systematic study of the intestinal flora , from a stool sample of a healthy young man from Senegal. Several species have also been isolated in addition to their occurrence in medical examination material from environmental samples, E. cancerogenus of trees, water and food, E. Kobei from foods and E. ludwigii from soil and plants. Other Enterobacter species have been isolated from plants and, according to the current state of knowledge, are typical of these, e.g. B. E. mori from the roots of a diseased mulberry tree Morus alba L. ( white mulberry ) or E. muelleri from the rhizosphere of Zea mays L. ( maize ).

meaning

biotechnology

Metabolic products of 2,3-butanediol fermentation
(S) -Acetolactate Structural Formula V1.svg
Acetolactate, acetyl lactate
(R) -acetoin.svg
Acetoin, 3-hydroxy-2-butanone
Butanedione - Butanedione.svg
Diacetyl, 2,3-butanedione

Certain Enterobacter enzymes can lead to a biotechnological use of the bacterium or its genes. The enzyme α-acetolactate decarboxylase ( acetyl lactate decarboxylase ) is used, for example, which causes the decarboxylation of acetyl lactate in 2,3-butanediol fermentation (acetyl lactate is also known as 2-acetolactate or α-acetolactate, it is the anion of the 2nd -Hydroxy-2-methyl-3-oxobutyric acid), whereby acetoin is formed. On the other hand, acetyl lactate can undergo oxidative decarboxylation without the action of enzymes and thereby be converted into diacetyl . Diacetyl is an organic compound which, in low concentration, has a pronounced taste and smell of butter and is also part of the natural butter aroma. On the other hand, it can lead to an off- flavor in wine and beer . Diacetyl can be enzymatically reduced to acetoin with the help of diacetyl reductase , which happens during the brewing process with the brewing yeast Saccharomyces cerevisiae . Nevertheless, small amounts of diacetyl can arise, which lead to the undesirable off-flavor. The gene for α-acetolactate decarboxylase was therefore transferred from Enterobacter by transformation into Saccharomyces cerevisiae . The recombinant yeast enabled the concentration of diacetyl in the wort to be reduced during the brewing process , as acetyl lactate was now converted directly into acetoin.

In contrast, diacetyl is also used as a flavoring substance , so that its biotechnological production is of interest. For this purpose, a strain of E. cloacae subsp. dissolvens the gene for the enzyme α-acetolactate decarboxylase "switched off" by gene knockout . In addition, the genes for the enzymes that reduce diacetyl to acetoin have been inactivated. The genetically modified bacteria then produced diacetyl in a fermenter . To increase the yield , the addition of iron (III) ions (Fe 3+ ions) has proven to be helpful. This increased the diacetyl concentration in the fermenter broth to 1.45 g / L.

Antibiotic resistance

An antibiotic resistance occurs when a particular bacterium resistant ( "resistant") to a particular antibiotic , it is therefore not inhibited by this growing. In other words, the antibiotic is not effective against the bacterium. In the case of bacteria, a distinction is sometimes made between natural (ly ) and acquired ( acquired ) resistance.

The representatives of the Enterobacter genus have a natural resistance to certain β-lactam antibiotics , as they have an inducible gene segment in their bacterial chromosome , the gene product of which is the enzyme cephalosporinase. Cephalosporinases are a subgroup of the β-lactamases that break down the β-lactam ring of this group of antibiotics, rendering them ineffective. Bacterial strains of the Enterobacter cloacae complex (including E. asburiae and E. hormaechei ) are therefore resistant to aminopenicillins and first generation cephalosporins . On the other hand, they are sensitive to carboxypicillins , some antibiotics are effective with 2nd generation cephalosporins and most antibiotics with 3rd generation cephalosporins. The gene called ampC codes for the enzyme called AmpC beta-lactamase (in this case a cephalosporinase). According to a study carried out in 2008, it is present in all Enterobacter isolates examined . A mutation can lead to overexpression of the AmpC-beta-lactamase encoded in the bacterial chromosome and, as a result, to resistance to cephalosporins of higher generations and cephamycins such as cefoxitin , cefotetan and cefmetazol .

The genes for acquired resistance are often located on a plasmid . This applies, for example, to the plasmid-coded penicillinase or the plasmid-coded extended spectrum β-lactamase ( ESBL ). Bacterial strains of the Enterobacter cloacae complex are able to inactivate carboxypenicillins (e.g. carbenicillin ) and ureidopenicillins ( mezlocillin ) as well as 3rd generation cephalosporins (e.g. cefotaxime ) through an acquired resistance . This means that they are resistant to two of the four antibiotic classes defined in the MRGN system (multi-resistant gram-negative bacteria). A multi-resistance is at Enterobacter spp. rather caused by overexpression of the chromosomally coded AmpC, a plasmid-coded ESBL also occurs. According to a report by the ECDC ( European Center for Disease Prevention and Control ), 32% of Enterobacter isolates showed resistance to 3rd generation cephalosporins in 2016 ; these data come from the European surveillance system TESSy.

Most recently, representatives of the Enterobacter genus were also reported that are resistant to carbapenems and thus to another of the four antibiotic classes defined in the MRGN system. Resistance to carbapenems is still rather rare and can be caused by the aforementioned AmpC-beta-lactamase or ESBL in combination with a loss of porin . But carbapenemase- producing representatives have also already been isolated. In Germany in 2010, VIM-1 (Verona-Integron-Metallo-β-Lactamase) was the most frequently identified carbapenemase in E. cloacae . According to the ECDC report, 2.6% of Enterobacter spp. Isolates showed resistance to carbapenems; 1,435 isolates from data from 14 countries collected as part of TESSy in 2016 were examined. The interim report on the European survey on carbapenemase-producing Enterobacteriaceae (EuSCAPE), also published by ECDC in 2013, provided data from 38 countries, according to which Enterobacter spp. Are present in Estonia and Lithuania . the dominant species in Enterobacteriaceae in terms of carbapenemase production. Most of the countries (33), however, named Klebsiella pneumoniae as the most important representative. The carbapenemases named after this bacterial species ( KPC-1 , KPC-2, etc.) are not limited to Klebsiella species, but can - as they are plasmid-coded - be exchanged between different gram-negative bacterial species by horizontal gene transfer . In 2004, Enterobacter isolates with a plasmid-coded KPC-2 β-lactamase (in this case a carbapenemase) were reported for the first time. The patient from whom the isolates were obtained was treated at a Boston hospital in 2001 and suffered from sepsis caused by various bacteria. The Enterobacter isolates, which were initially unspecified, were identified as E. cloacae or E. asburiae using various test methods , although an exact assignment was not possible.

While in 1970 all E. cloacae strains were sensitive to gentamicin , an aminoglycoside antibiotic , that changed rapidly in the course of the 1970s. The reason for this are the AME genes located on a plasmid, which code for the aminoglycoside-modifying enzymes that change the structure of this group of antibiotics in such a way that they are no longer effective. In addition to gentamicin, u. a. Tobramycin and Amikacin affected.

Antibiotic resistance is determined in the laboratory using an antibiogram . The Kirby-Bauer method is often used, in which, in an agar diffusion test, small circular filter plates containing various antibiotics are placed on Müller-Hinton agar with a distributed suspension of the bacterium. Several initial descriptions of Enterobacter species contain the results of these antibiograms, for example E. bugandensis , E. hormaechei and E. massiliensis .

The PCR method can also be used. It targets the genes that are responsible for the antibiotic resistance of the bacteria, as they encode the enzymes that break down or modify the antibiotics and thus render them ineffective. In 2015, 77 Enterobacter isolates that were involved in nosocomial infections (“hospital infections”) in Algeria (27 samples) and France (50 samples) and which were assumed to be E. cloacae were tested using PCR . The PCR method showed that 29 isolates had at least one ESBL-coding gene and 28 isolates had AME genes (aminoglycoside-modifying enzymes). The relative and absolute frequency of positive results was greater for the samples from Algeria (18 and 20) than for those from France (11 and 8).

Medical importance

The human medical relevance of the species remaining in the genus is still the subject of research. It is believed that, in addition to the cases of infectious diseases caused by Enterobacter species mentioned in the section on pathogenicity , they also affect infectious diseases of the lower respiratory tract , pneumonia , infectious diseases of the skin and soft tissue , and ophthalmic (the eye) infectious diseases , Endocarditis as well as septic arthritis can be responsible. Most of the cases are hospital-acquired (nosocomial) infections. Species isolated from medical specimens in hospital or related to nosocomial infectious diseases are considered opportunistic pathogens . The problem is the widespread resistance to several antibiotics, so that they are of increasing importance as pathogens for nosocomial infectious diseases. In contrast, unlike Cronobacter sakazakii , Enterobacter species play no epidemiological role in food infections.

Infections that occur in hospitals mainly affect immunosuppressed patients. Furthermore, newborns are at risk for whom the criteria of premature birth , low birth weight, use of invasive medical procedures and excessive use of antibiotics are risk factors. E. cloacae and E. hormaechei are associated with neonatal infectious diseases , as well as C. sakazakii ( necrotizing enterocolitis in Cronobacter infections), K. aerogenes and Pluralibacter gergoviae , which no longer belong to the genus . It should be noted here that in the past incorrect results have frequently been obtained with regard to the distinction between E. hormaechei and Cronobacter species. Pneumonias are v. a. Intensive care ventilated patients affected. A report by the ECDC named Enterobacter species as the cause of 10% of lung infections acquired in an intensive care unit in 2016 (for comparison: Pseudomonas aeruginosa 21%, Staphylococcus aureus 18%, Klebsiella spp. 16% and Escherichia coli 13%).

In the case of infections with Enterobacter species, an antibiogram should first be carried out to clarify the resistance. Often, 3rd generation ureidopenicillins and cephalosporins (e.g. cefotaxime and ceftazidime ) are used, but they are not effective in multi-resistant species that have a plasmid-coded penicillinase or the plasmid-coded extended spectrum β-lactamase . Other antibiotics used are carbapenems, quinolones and aminoglycosides. Carbapenems are recommended for Enterobacter species that are resistant to the chromosomally coded AmpC-beta-lactamase (in this case a cephalosporinase), although it should be noted that resistance to this group of antibiotics can also occur.

Most of the data on medical significance can be found on the type species E. cloacae . In 1966 it was reported that she colonized patients in hospital by accident rather than being responsible for an infection. In the 1970s, it was assumed that a particular E. cloacae strain was endemic to a particular hospital and that it was an opportunistic pathogen that caused infectious diseases in immunocompromised patients. Hygiene studies have shown that the strain is spread via contaminated hands of the nursing staff and that cross-contamination occurs via medical devices and liquids (e.g. the water used in hydrotherapy , but also disinfectants with benzalkonium chloride ) . According to statistics from the Centers for Disease Control and Prevention (CDC), E. cloacae was responsible for 4.6% in 1975 and 5.9% of nosocomial infectious diseases in US hospitals in 1984.

Monitoring programs

In order to collect epidemiologically useful information about infectious diseases and the pathogens involved, there are various monitoring programs (so-called Surveillances). In 2015, the Robert Koch Institute (RKI) published an overview of the surveillance systems for pathogens and resistance for Germany. It lists the surveillance of antibiotic use and bacterial resistance in intensive care units (SARI), which is organized by the National Reference Center for Surveillance of Nosocomial Infections at the Institute for Hygiene and Environmental Medicine, Charité Berlin and the Institute for Environmental Medicine and Hospital Hygiene at the University of Freiburg . In the SARI program, samples are examined for 13 common pathogens and their antibiotic resistance; E. cloacae is one of the bacteria listed . The participation of hospitals in this surveillance is voluntary. In contrast, the provisions of the Infection Protection Act (IfSG) are mandatory. For example, Section 23  IfSG stipulates that nosocomial infectious diseases and pathogens with special and multi- resistances are to be recorded. The further details are determined by the anti-infectives, resistance and therapy commission set up at the Robert Koch Institute and published in a list in the Federal Health Gazette. There is also among the listed bacteria E. cloacae to find to be detected, provided that a single resistance to imipenem or meropenem was observed, or a multi-resistance according to the KRINKO definition for 3 MRGN or 4MRGN. The abbreviation KRINKO stands for the Commission for Hospital Hygiene and Infection Prevention, also set up at the RKI .

Monitoring systems have also been set up internationally, for example the European survey on carbapenemase-producing Enterobacteriaceae (EuSCAPE). The 28 member states of the European Union , Iceland, Norway, seven (potential) candidate countries and Israel are involved in this surveillance system . An interim report published in 2013 indicates that 28 of these 38 states maintain a national surveillance system for carbapenemase-producing Enterobacteriaceae (CPE), of which Enterobacter spp. Is also used in 24 national programs . supervised. Another European surveillance system is called TESSy (The European Surveillance System) and provides data on nosocomial infections, which are published annually as surveillance reports by the ECDC and which also take into account Enterobacter species.

In the case of information on the occurrence of infectious diseases caused by Enterobacter species, the diagnostically difficult differentiation between the species and the related genera such as Klebsiella and Cronobacter must be taken into account. According to a report by the German Hospital Infection Surveillance System (KISS), Enterobacter species were responsible for 6.5% of all nosocomial infectious diseases in intensive care units in 2011. Data from surveillance programs and case studies of outbreaks of infectious diseases in intensive care units are available for North and South America, Europe and Asia.

swell

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Individual evidence

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This article was added to the list of excellent articles on June 16, 2018 in this version .