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The Enterobacteriaceae: general characteristics J.J. FARMER III, M.K. FARMER, AND BARRY HOLMES Introduction 1 Isolation 31 Nomenclature and classification 15 Identification 31 Cell structure and cellular antigens 23 Typing methods 36 Nutrition and growth 28 Antibiotic sensitivity and resistance 36 Hab...

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The Enterobacteriaceae: general characteristics Carlos Vazquez

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The Enterobacteriaceae: general characteristics J.J. FARMER III, M.K. FARMER, AND BARRY HOLMES Introduction Nomenclature and classification Cell structure and cellular antigens Nutrition and growth Habitats Human infections, pathogenicity, and virulence

1 15 23 28 30 30

INTRODUCTION The family Enterobacteriaceae is one of the most important bacterial families. It includes the plague bacillus Yersinia pestis and the typhoid bacillus Salmonella serotype Typhi (Salmonella typhi) which are two of the most important bacterial pathogens in human history. It also includes two genera of intrinsic enteric pathogens Shigella and Salmonella; essentially all strains in these two genera can cause diarrhea or intestinal infections (Centers for Disease Control and Prevention (Anonymous) 2003). Two other genera, Escherichia (Gamage et al. 2003; Misselwitz et al. 2003; Naimi et al. 2003; Riley et al. 1983; Vallance et al. 2002) and Yersinia, also include enteric pathogens; however, only a few of the many serotypes (strains) have the virulence factors that enable them to infect the intestinal tract or allow them to colonize it and produce enterotoxins. Many other species have an association with diarrhea (Murata et al. 2001), but their causal role is uncertain. Several other species of Enterobacteriaceae frequently cause extraintestinal human infections (Diekema et al. 1999; Edmond et al. 1999; O’Hara et al. 2000a) and some have an association with chronic diseases such as arthritis (Yu and Kuipers 2003). Many other species occasionally cause infections or occur in human clinical specimens, and often it is difficult to determine their clinical signifi-

Isolation Identification Typing methods Antibiotic sensitivity and resistance Literature and the internet Acknowledgments References

31 31 36 36 38 39 39

cance. Other genera and species do not cause disease or occur in human clinical specimens, but can be confused with those species that do. The family also includes plant and animal pathogens and a number of species that have been favorite subjects for studies on genetics, physiology, metabolism, antibiotic resistance, ecology, epidemiology, pathogenicity, virulence, and vaccines. In this tenth edition of Topley and Wilson, the material on Enterobacteriaceae is divided in a manner similar to the ninth edition. One difference is that the chapter Escherichia and Shigella has been divided; each genus now has its own chapter. A second difference is that Plesiomonas is now classified in the family (see section entitled Inclusion of the genus Plesiomonas); in previous editions, this oxidase-positive species was included in chapters with two oxidase-positive relatives, Vibrio and Aeromonas. The introductory chapter on Enterobacteriaceae has changed only slightly over the last several editions of this book; however, our revision is a major one. We have updated some of the material covered in the ninth edition, but felt that it was equally important to add new sections and recent references. Because of space limitations and because they are fully discussed in the following six chapters ( Escherichia; Shigella; Salmonella; Proteus, Morganella, and Providencia;

2

The Enterobacteriaceae: general characteristics

Yersinia; and Citrobacter, Klebsiella, Enterobacter, Serratia, and other Enterobacteriaceae), many topics in the present chapter are only briefly mentioned. The statement ‘see . . . in the chapter(s) that follows for more details and references’ is implied in every instance. Many other chapters in the tenth edition have useful information on the Enterobacteriaceae. Those chapters of particular interest are the ones that cover: history; cell structure and function; taxonomy and nomenclature; diversity; genetics; bacteriophages; antibiotics; water; milk and foods; normal flora; pathogenicity and virulence; typhoid and paratyphoid; bacillary dysentery; E. coli diarrhea; acute enteritis; food-borne illnesses; food poisoning; plague and other Yersinia infections; infections of the urinary tract; and hospitalacquired infections. For a historical approach to the family and for invaluable basic information on isolation, identification, and serotyping, the classic books by Edwards and Ewing (1972), Ewing (1986), and Kauffmann (1969) are essential reading. The more recent book The Enterobacteria by Janda and Abbott (1998) covers the whole family, and is also highly recommended. Other books and encyclopedias (Lederberg 2000) cover many specific topics such as basic biology, nomenclature, and classification (Boone et al. 2001; Brenner et al. 2005), laboratory media and methods (Atlas and Parks 1997; Balows et al. 1988; Murray et al. 2003), infectious diseases (Farthing and Keusch 1988; Mandell et al. 2000), and hospital (nosocomial) infections (Mayhall 2000). Also, try searching www.booksinprint.com (not free, but available in many libraries). Several reviews and chapters also cover the entire family and are recommended (Balows et al. 1992; Brenner 1992a, b, 1984; Brenner and Farmer 2005; Farmer et al. 1985; Farmer 2003; Krieg 1984). Many articles, books, chapters, reviews, and internet sites cover the individual genera and species in the family, and are discussed in the following six chapters (Chapters 52–57).

Phenotypic definition Most genera and species in the family Enterobacteriaceae share the following properties: they are small gram-negative rods; do not have unusual cell structures or produce spores; are motile by peritrichous flagella; grow on ordinary laboratory media formulated with peptones or meat extracts; grow both aerobically and anaerobically; grow without the addition of sodium chloride or other supplements; grow well on MacConkey agar; are active biochemically; ferment D-glucose and other sugars, often with gas production; are catalase positive and oxidase negative; reduce nitrate to nitrite; contain the enterobacterial common antigen (eca); and have a 39–59 percent guanine-plus-cytosine (G + C) content of DNA (Balows et al. 1992; Brenner et al. 2005), with most of the genera in the range 49–59 mol%.

Table 1 expands on this definition, and gives quantitative data and the exceptions. It also lists the species most frequently isolated from human and animal diseases and those that occur in clinical specimens. Table 2 (p. 14) compares Enterobacteriaceae with three genera that are close relatives. Host-adapted species that are uncultivable, difficult to culture, or slow growing have evolved in some genera (Table 3, p. 14). A number of new or unusual species that have not yet been isolated from human clinical specimens have been reported (Table 3).

Molecular and genetic definition, relatives, population structure, and evolution When techniques such as DNA–DNA hybridization and 16S r-RNA sequencing (Fox et al. 1992; Stackebrandt and Goebel 1994) that measure evolutionary distance are used, genera and species in the family are more closely related to Escherichia coli, the type species of the type genus of the family, than they are to organisms in other families. The phylogenetic position of the family Enterobacteriaceae is in the gamma subclass of Proteobacteria, a subclass also known as the ‘purple bacteria’ (Figures 1 and 2, pp. 15 and pp. 16). The figures show that the closest relatives of Enterobacteriaceae are the families Alteromonadaceae, Vibrionaceae, Aeromonadaceae, and Pasteurellaceae. The use of DNA–DNA hybridization (Brenner and Farmer 2005; Brenner 1984; Farmer et al. 1985) has greatly expanded the number of species in the family and has led to a basic understanding of the phylogenic relationship of the genera and species (Boyd et al. 1996; Brunder and Karch 2000; Ochman and Groisman 1995; Oelschlaeger et al. 2002; Oyston et al. 2003; Szakal et al. 2003; Vallance et al. 2002; Vulic et al. 1997). 16S rRNA sequencing data have been very helpful in defining phylogenetic relationships at the level of genus and family. Multilocus enzyme electrophoresis (MEE) has been used to define population structure and evolutionary relationships in Escherichia coli–Shigella (Dobrindt et al. 2003; Neidhardt 1996), Salmonella (Neidhardt 1996), Yersinia, and in several other genera, species, and serotypes. Several evolutionary pathways are now understood: the evolution of Shigella from Escherichia coli; the evolution of Escherichia coli O157 from Escherichia coli O55:H7 (Whittam et al. 1993) and the evolution of Yersinia pestis from Yersinia pseudotuberculosis which happened relatively recently.

History An excellent way to follow the history of the family Enterobacteriaceae is to start with the first edition of Topley & Wilson and follow the evolution of genus and species names and individual topics through its ten

100 100 100 100 100 100 100 100 100 100 100 100 100 100 100 100 100 100 100 100 100 100 100 100 100 100 100

53 100 100 100 40 100 100 100 70 100 100 100 100 89 98 97 96 75 93 100 100 100 100 100 100 50 35

87 100 0 0 60 100 0 0 19 60 35 0 0 78 50 35 15 25 80 17 100 100 67 67 0 0 0

0 0 0 0 0 0 0 0 100 0 100 50 100 89 40 9 100 20 7 0 0 0 33 33 0 100 100

60 100 100 100 100 100 100 100 100 100 100 100 100 100 99 100 100 100 100 100 100 100 100 100 0 100 100

0 0 0 0 0 0 0 0 0 0 0 0 0 11 40 1 2 85 33 0 100 0 0 100 0 0 0

0 100 100 100 100 100 100 100 99 100 100 100 100 0 15 30 9 10 0 0 17 0 0 33 0 0 50

0 0 67 0 100 0 0 0 0 0 0 0 0 0 99 0 0 0 0 0 0 0 0 0 0 0 0

0 0 0 0 0 0 0 67 0 0 0 0 0 0 0 0 0 5 0 0 0 0 0 0 0 0 0

fermentation

Adonitol fermentation

0 60 100 0 100 100 100 100 91 99 100 0 0 11 95 1 0 5 0 100 100 100 100 0 0 0 100

D-Sorbitol

Salicin fermentation

0 80 100 40 60 67 100 33 86 100 65 100 100 89 0 99 93 95 100 100 100 0 100 100 0 0 0

myo-Inositol fermentation

Dulcitol fermentation

fermentation D-Mannitol

0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0

Sucrose fermentation

27 100 100 60 80 100 100 100 95 80 100 100 100 89 95 95 97 95 87 100 100 0 67 100 98 100 100

Lactose fermentation

0 100 33 80 0 100 0 0 95 0 0 0 50 0 99 95 100 5 93 0 100 100 0 0 100 100 95

gas

0 0 0 0 20 0 67 0 50 80 100 100 50 67 80 85 85 50 67 100 100 0 33 67 0 0 0

D-Glucose,

0 0 0 100 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 100 100 100

acid

Motility

0 0 0 0 0 0 100 100 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0

D-Glucose,

Ornithine decarboxylase

33 0 0 0 0 0 0 0 0 0 0 0 0 44 75 85 59 80 47 100 100 100 0 67 0 0 0

Malonate utilization

Arginine dihydrolase

80 0 0 0 0 0 0 0 0 0 0 0 0 78 0 5 0 65 60 100 0 0 67 67 100 0 0

Growth in KCN

Lysine decarboxylase

0 100 0 0 20 0 33 33 95 99 100 100 100 78 99 95 10 75 87 100 83 0 33 100 1 0 0

Gelatin hydrolysis (22
C)

Phenylalanine deaminase

0 0 0 0 0 0 0 0 50 80 50 50 50 0 0 0 0 0 0 0 0 0 0 0 0 0 0

Urea hydrolysis

93 100 100 100 100 100 100 100 100 40 100 100 100 100 100 100 100 100 100 100 100 100 100 100 100 100 100

Hydrogen sulfide (TSI)

0 0 0 0 0 0 33 0 0 0 0 0 0 33 99 100 100 15 33 0 83 0 0 100 99 100 50

Citrate (Simmons)

Methyl red

Budvicia aquatica*b Buttiauxella agrestis Buttiauxella brennerae Buttiauxella ferragutiae Buttiauxella gaviniae Buttiauxella izardii Buttiauxella noackiae* Buttiauxella warmboldiae Cedecea davisae* Cedecea lapagei* Cedecea neteri* Cedecea species 3* Cedecea species 5* Citrobacter freundii* Citrobacter diversus (C. koseri)* Citrobacter amalonaticus* Citrobacter farmeri* Citrobacter youngae* Citrobacter braakii* Citrobacter werkmanii* Citrobacter sedlakii* Citrobacter rodentium* Citrobacter gillenii* Citrobacter murliniae* Edwardsiella tarda* Edwardsiella tarda biogroup 1* Edwardsiella hoshinae*

Voges Proskauer

Organism

Indole production

Table 1 Biochemical reactions a of the named species, subspecies, biogroups, and enteric groups of the family Enterobacteriaceaea,b

0 0 0 100 0 0 0 0 0 0 100 0 100 100 99 99 98 100 100 100 100 100 100 100 0 0 0 3

(Continued over)

fermentation

myo-Inositol fermentation

Adonitol fermentation

100 98 0 0

0 0 97 0

65 98 96 0

0 97 95 85

0 0 0 2

0 98 98 35

0 95 75 65

100 100 100 100

50 100 100 20

0 95 93 40

0 100 97 75

0 100 100 100

0 5 15 15

0 100 75 65

0 98 25 7

0 95 15 15

0 100 95 30

0 11 0

5 5 5

100 100 100

99 99 100

0 0 0

93 1 1

0 50 0

90 0 0

0 99 94

100 91 99

90 96 99

0 0 0

0 99 98

96 18 100

100 100 100

98 98 100

55 99 10

98 100 0

99 100 100

0 5 0

99 99 92

0 0 0

0 75 0

0 0 1

0

7

100

70

0

0

0

0

9

55

92

0

100

91

100

100

70

100

100

0

91

0

0

9

0

65

100

100

0

0

0

0

35

100

100

0

100

100

100

100

35

0

100

0

100

0

0

100

0 0 0 0 0 0 0 98 80 98 99 0 0 45 50

100 57 100 0 0 100 29 99 95 100 100 100 100 99 100

2 100 100 100 100 100 86 0 0 0 0 0 0 0 0

100 96 65 100 100 0 0 1 1 17 1 0 50 0 0

0 0 0 0 0 0 0 1 1 0 0 0 0 0 0

60 87 0 0 100 0 86 1 1 0 0 0 0 0 0

0 4 0 0 0 0 0 0 0 0 0 0 0 0 0

0 0 0 0 0 0 100 90 40 95 6 85 100 0 0

21 78 0 100 100 0 0 17 3 5 0 30 0 2 5

95 91 89 100 100 100 100 65 20 100 100 0 100 0 0

0 52 89 100 0 0 43 95 5 93 99 100 0 0 0

0 0 0 0 0 0 0 0 0 0 0 0 0 0 0

97 100 65 100 100 100 0 3 1 0 94 15 0 0 0

3 100 100 100 100 100 86 0 0 35 0 85 100 0 0

100 100 100 100 100 100 100 100 100 100 100 100 100 100 100

95 83 100 100 100 100 100 95 5 95 97 97 100 0 3

75 9 100 0 0 0 14 95 25 0 45 15 0 0 1

100 100 65 0 100 0 100 50 15 0 45 8 0 0 1

100 100 100 100 100 100 100 98 93 98 100 100 0 0 95

0 87 100 0 0 0 0 60 40 60 19 0 0 5 1

100 44 100 100 100 100 100 40 10 65 40 30 0 0 0

0 0 0 0 0 0 0 5 3 98 0 0 0 0 0

0 0 0 0 0 0 100 1 1 0 0 0 0 0 0

100 0 100 0 100 100 0 94 75 0 0 1 0 30 29

Arginine dihydrolase

Methyl red

D-Sorbitol

0 0 0 20

Salicin fermentation

D-Mannitol

Dulcitol fermentation

Sucrose fermentation

fermentation

gas D-Glucose,

0 2 65 20

Lactose fermentation

acid

0 0 0 0

Malonate utilization

0 95 100 50

Growth in KCN

0 98 100 70

Motility

0 5 5 50

Lysine decarboxylase

D-Glucose,

Gelatin hydrolysis (22
C)

Ornithine decarboxylase

Phenylalanine deaminase

0 0 0 20

Urea hydrolysis

Citrate (Simmons)

Hydrogen sulfide (TSI)

Voges Proskauer

Edwardsiella ictaluri Enterobacter aerogenes* Enterobacter cloacae complex* ’Enterobacter agglomerans complex’* Enterobacter gergoviae* Enterobacter sakazakii* Enterobacter taylorae (E. cancerogenus)* Enterobacter amnigenus biogroup 1* Enterobacter amnigenus biogroup 2* Enterobacter asburiae* Enterobacter hormaechei* Enterobacter intermedius* Enterobacter cancerogenus Enterobacter dissolvens Enterobacter nimipressuralis Enterobacter pyrinus Escherichia coli* Escherichia coli, inactive* Escherichia fergusonii* Escherichia hermannii* Escherichia vulneris* Escherichia blattae Shigella dysenteriae (Group A)* Shigella flexneri (Group B)*

Indole production

Organism

4

Table 1 Biochemical reactions a of the named species, subspecies, biogroups, and enteric groups of the family Enterobacteriaceaea,b (Continued )

(Continued over)

Ornithine decarboxylase

Growth in KCN

Malonate utilization

acid

gas

Motility

D-Glucose,

D-Glucose,

Lactose fermentation

Sucrose fermentation

D-Mannitol

Salicin fermentation

Adonitol fermentation

myo-Inositol fermentation

D-Sorbitol

0 0 95 10 0 98 95 100 100 30 0 40 96 80 100 0 100 0 80 0

0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 100 100 0 20

0 0 0 4 0 95 90 100 98 10 0 0 0 0 0 48 0 0 0 95

0 0 0 0 0 0 1 0 0 0 0 0 0 0 0 0 0 0 0 95

0 0 0 100 100 98 99 100 100 40 0 100 97 23 100 0 0 0 0 1

18 2 0 6 0 0 0 0 0 6 0 0 0 0 0 0 0 0 0 0

2 98 0 98 45 0 0 100 0 3 0 20 100 100 100 0 0 0 0 95

0 0 60 85 0 0 0 0 0 0 0 0 98 90 100 79 0 0 0 95

0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0

0 0 5 95 0 98 97 100 100 88 80 100 92 86 83 97 0 0 70 98

0 0 0 50 45 93 98 100 100 3 95 100 96 86 50 93 0 0 0 1

100 100 100 100 100 100 100 100 100 100 100 100 100 100 100 100 100 100 100 99

0 0 0 98 0 97 97 100 100 50 0 80 93 95 17 97 33 0 0 90

1 2 70 5 0 98 100 100 100 30 0 100 98 95 83 93 0 0 100 1

0 1 0 10 0 99 100 100 100 20 75 100 98 81 100 66 0 0 100 0

97 99 100 99 55 99 99 100 100 100 100 100 100 95 100 100 0 0 60 0

5 0 0 0 0 30 55 10 15 2 0 20 25 0 33 86 83 0 0 0

0 0 80 13 55 99 100 100 100 97 98 100 100 100 100 100 0 0 0 0

0 0 0 0 0 90 99 100 100 97 100 100 0 0 0 93 0 0 100 0

0 0 0 0 0 95 98 95 100 55 95 80 0 0 0 0 0 0 0 0

43 2 0 0 0 99 99 100 92 65 100 100 40 45 0 0 0 0 0 0

100 50

95 86

0 0

0 0

15 7

100 100

100 93

100 29

0 0

80 64

0 79

0 0

90 79

5 0

100 100

93 86

0 0

0 7

0 0

0 0

0 0

0 0

0 0

0 0

0

15

0

0

0

0

0

100

0

100

0

0

0

0...