The Genus Serratia

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222 F. Grimont and P.A.D. Grimont CHAPTER 3.3.11 cause fig spoilage. Washing of a syconium cavity can yield 10 to 300 colony-forming-units (CFU) of S. ficaria. Serratia rubidaea has been repeatedly isolated from coconuts bought in France (originating mostly from Ivory Coast) and in California (Grimont et al., 1981). The three subspecies (former biotypes B1 to B3) have been associated with coconuts, and when present, S. rubidaea numbered 3× 10 4 to 6× 10 6 CFU per gram of coconut milk or flesh (Bollet et al., 1989). It is believed that coconut palms have been disseminated worldwide from an Indo-Pacific origin. It would thus be interesting to compare the bacterial flora of coconuts collected in diverse countries. In the course of an ecological survey and using the selective caprylate-thallous agar medium, Serratia species were frequently found associated with plants (Grimont et al., 1981). With respects to the presence of Serratia, plants (other than figs and coconuts) were classified into three prevalence groups. In the first group, which is composed of vegetables, mushrooms, mosses, and decaying plant material (i.e., wet plants), about 54% of the samples carried Serratia in counts varying from 2,000 to over 20,000 CFU per gram of plant (highest counts in mushrooms and leaves of radish, lettuce, cauliflower, and brussels sprout). In the second group, which is composed of grasses, Serratia prevalence was about 24%. In the third group composed of trees and shrubs, 8% of the samples (leaves) contained Serratia (10 to 300 CFU per gram). Serratia strains isolated from plants other than figs and coconuts were distributed among eight Serratia species, although S. liquefaciens and S. proteamaculans were predominant (Table 1). The selective medium used (caprylate-thallous agar) was unable to support the growth of S. fonticola. S. entomophila was not isolated although this species can grow on the selective medium. Pigmented S. marcescens biotypes were rarely isolated from plants. Nonpigmented S. marcescens biogroups A3 and A4 were isolated from plants, but biogroups A5/8 and TCT were not (Table 2). Vegetables used in salads might bring Serratia strains to hospitals and contaminate the patient’s digestive tract. S. marcescens, S. liquefaciens, and S. rubidaea were found in 29%, 28%, and 11% (respectively) of vegetable salads served in a hospital in Pittsburgh (Wright et al., 1976). Similar results were found in a Paris hospital (Loiseau-Marolleau and Laforest, 1976). However, it still needs to be proven that biotypes/ serotypes found in patients are the same as those found in salads. In the first described case of S. ficaria infection, the patient was very fond of figs (Gill et al., 1981). Serratia in Insects There is an extensive literature on Serratia associated with insects. This topic has been reviewed in detail (Bucher, 1963a; Grimont and Grimont, 1978a; Steinhaus, 1959). The insects involved belong to numerous species and genera of the orders Orthoptera (crickets and grasshoppers), Isoptera (termites), Coleoptera (beetles and weevils), Lepidoptera (moths), Hymenoptera (bees and wasps), and Diptera (flies). Taxonomic uncertainties make a retrospective evaluation of the role of Serratia spp. in insect infections difficult. Red-pigmented Serratia were easily recognized (although not determined as to species with any certainty), whereas nonpigmented strains were often referred to genera other than Serratia. For example, S. proteamaculans or S. liquefaciens strains were named “Bacillus noctuarum” (White, 1923b), “Bacillus melolonthae liquefaciens” (Paillot, 1916), “Paracolobactrum rhyncoli” (Pesson et al., 1955), and “Cloaca” B type 71–12A (Bucher and Stephens, 1959); nonpigmented S. marcescens strains were named “Bacillus sphingidis” (White, 1923a) and “Bacillus apisepticus” (Burnside, 1928). The distribution among the various Serratia species of 48 collection strains isolated from insects (Grimont et al., 1979b) showed a predominance of S. marcescens and S. liquefaciens. The absence of S. plymuthica (a pigmented species) in this collection is unexplained. Steinhaus (1941) reported the presence of S. plymuthica in the gut of healthy crickets (Neombius fasciatus), but the taxonomic schemes in vogue at that time did not allow a definite identification of S. plymuthica. The rarity of S. rubidaea (also a pigmented species) in insects might be explained by its inability to produce chitinase—a virulence factor for insect-associated Serratia species (Lysenko, 1976). The red-pigmented Serratia isolates associated with the fig wasp Blastophaga psenes and formerly identified as S. plymuthica (Phaff and Miller, 1961) were reidentified as S. marcescens biotype A1b (Grimont et al., 1981). It is noteworthy that S. ficaria was isolated from both the fig wasp Blastophaga psenes and from a black ant, i.e., Hymenoptera (Grimont et al., 1979c). S. liquefaciens and S. marcescens were found in sugar-beet root-maggot development stages (Tetanops myopaeformis), suggesting an insectmicrobe symbiosis, as well as a nutritional interdependence (Iverson et al. 1984). A relationship appeared to exist between adult fly emergence and enzymatic chitin degradation of the puparium by the bacterial symbionts. S. marcescens biotype A4b was repeatedly isolated from diseased honeybee (Apis mellifera) larvae in Sudan (El Sanoussi et al., 1987).
CHAPTER 3.3.11 The Genus Serratia 223 Serratia marcescens, S. proteamaculans and S. liquefaciens are considered potential insect pathogens (Bucher, 1960). They cause a lethal septicemia after penetration into the hemocoel. More than 70 species of insects were found to be susceptible to inoculation with Serratia (Bucher, 1963a). The lethal dose (LD 50) of inoculated Serratia (by intrahemocoelic injection) was calculated for several insects 10–50 Serratia cells per grasshopper (Bucher, 1959), 5.1 cells per adult bollweevil (Slatten and Larson, 1967), 7.5 and 14.5 cells per third and fourth instar larva (respectively) of Lymantria dispar (Podgwaite and Cosenza, 1976), and 40 cells per Galleria mellonella larva (Stephens, 1959). The LD 50 of ingested S. marcescens is much higher. The hemolymph of insects—normally bactericidal for nonpathogens—cannot prevent multiplication of potential pathogens (Stephens, 1963). Lecithinase, proteinase, and chitinase play a role in the virulence of Serratia for insects, and purified Serratia proteinase or chitinase is very toxic when injected into the hemocoel (Kaska, 1976; Lysenko, 1976). Serratia strains in the insect digestive tract probably originate from plants. The multiplication of Serratia strains in the insect digestive tract has not been quantitatively studied. Antibacterial substances in ingested leaves might interfere with bacterial multiplication, but Serratia strains were found resistant to these (Kushner and Harvey, 1962). How potential pathogens such as Serratia can enter the hemolymph from the gut is generally unknown. However, spontaneous gut rupture, which happens in about 10% of grasshoppers, may allow Serratia strains to invade the hemocoel (Bucher, 1959). Direct injection occurs when Itoplectis conquisitor contaminated with Serratia stings host pupae to oviposit into their bodies (Bucher, 1963b). Serratia epizootics are common among reared insects (Bucher, 1963a). However, until recently, no genuine epizootic of Serratia infection among insects had been observed in the field. Strains of S. entomophila and S. proteamaculans can be pathogenic for the grass grub Costelytra zealandica, which is a major pasture pest in New Zealand (Stucki and Jackson, 1984; Trought et al., 1982). Larvae of Costelytra zealandica feed on grass, clover, and other plant roots. Typically, their populations grow to a peak (about 600 larvae/m 2 ) in 4 to 6 years after the pasture is sown and then collapse (to about 50 larvae/m 2 ). Grass grub population collapse was found associated with the presence of a disease called amber disease (Trought et al., 1982). S. entomophila and S. proteamaculans were isolated from naturally infected larvae and shown experimentally to produce the disease when transmitted orally to healthy larvae (Grimont et al., 1988; Stucki and Jackson, 1984). The bacteria are ingested from the soil. Infected larvae stop feeding within a few days, become translucent and then amber colored and lose weight until death occurs 4 to 6 weeks later. The bacteria colonize the gut and cause disease symptoms without invading the hemocoele. Field trials have shown that control of the grass grub was feasible by application of S. entomophila suspensions on pastures (Jackson and Pearson 1986). Reductions of 30 to 59% in the larval populations were obtained, with 47% of the remaining larvae being infected. Such bacterial treatment resulted in a 30% increase in grass production (dry matter). Serratia in Vertebrates Serratia has been associated with chronic infections of cold-blooded vertebrates: nodular infection of Anolis equestris, the Cuban lizard (Duran-Reynals and Clausen, 1937); subcutaneous abscess of iguanid lizards (Boam et al., 1970); arthritis in the lizard Tupinambis tequixin (Ackerman et al., 1971); and ulcerative disease in the painted turtle Chrysemys picta (Jackson and Fulton, 1976). Serratia strains have also been recovered from the healthy, small, green pet turtle Pseudemys scripta elegans (McCoy and Seidler, 1973) and from geckos and turtles in Vietnam (Capponi et al., 1956). Poultry may be contaminated with Serratia. A deadly Serratia epizootic among chick embryos was observed in a Japanese hatchery (Izawa et al., 1971). The hens carried S. marcescens in their digestive tract, but were themselves unaffected. Contamination of chicken carcasses with S. liquefaciens (Lahellec et al., 1975) and spoilage of eggs by red-pigmented Serratia (Alford et al., 1950) have been reported. A disseminated suppurative infection in a blue and gold macaw (Ara ararauna) affected with a chronic lymphoid atrophy has also been recorded (Quesenberry and Short, 1983). Serratia strains (mostly red-pigmented) are responsible for 0.2–1.5% of cases of mastitis in cows (Barnum et al., 1958; Roussel et al., 1969; Wilson, 1963). Raw milk, therefore, may occasionally contain Serratia spp., and S. liquefaciens and S. grimesii are common in dairy products (Grimes and Hennerty, 1931). Serratia strains have been involved in septicemia in foals (Deom and Mortelmans, 1953), goats (Wijewanta and Fernando, 1970), and pigs (Brisou and Cadeillan, 1959); they have also been implicated in conjunctivitis of the horse (Carter, 1973) and abortion in cows (Smith and Reynolds, 1970). The isolation of Serratia from the anal sac of the red fox Vulpes vulpes (Gosden and Ware, 1976) has been reported. Serratia strains have rarely been systematically searched for in the gut of animals. S. fonticola
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