Abstract
Capnocytophaga canimorsus, a commensal bacterium of the canine oral flora, has been repeatedly isolated since 1976 from severe human infections transmitted by dog bites. Here, we show that C. canimorsus exhibits robust growth when it is in direct contact with mammalian cells, including phagocytes. This property was found to be dependent on a surface-exposed sialidase allowing C. canimorsus to utilize internal aminosugars of glycan chains from host cell glycoproteins. Although sialidase probably evolved to sustain commensalism, by releasing carbohydrates from mucosal surfaces, it also contributed to bacterial persistence in a murine infection model: the wild type, but not the sialidase-deficient mutant, grew and persisted, both when infected singly or in competition. This study reveals an example of pathogenic bacteria feeding on mammalian cells, including phagocytes by deglycosylation of host glycans, and it illustrates how the adaptation of a commensal to its ecological niche in the host, here the dog's oral cavity, contributes to being a potential pathogen.
Highlights
Capnocytophaga canimorsus has been rarely but regularly isolated from dog or cat bite infections since its discovery in 1976 [1,2]
When inoculated at a multiplicity of infection of 20 to J774.1 murine macrophages cultured in complete RPMI, which includes 10% fetal bovine serum (FBS), C. canimorsus 5 (Cc5) multiplied about 100-fold during the 24 h of infection (Fig. 1A)
Growth was abolished when J774.1 macrophages were omitted and Cc5 was unable to grow in a transwell system, indicating that direct contact is required for bacterial growth (Fig. 1B)
Summary
Capnocytophaga canimorsus (formerly Centers for Disease Control group DF-2) has been rarely but regularly isolated from dog or cat bite infections since its discovery in 1976 [1,2]. The family of Flavobacteriaceae includes a variety of environmental and marine bacteria, among which Flavobacterium johnsoniae is a common soil and freshwater bacterium studied for its gliding motility [7]. There are only a few examples of pathogenic bacteria belonging to this family These are Flavobacterium psychrophilum, the causative agent of cold water disease in salmonid fish [8], Ornithobacterium rhinotracheale, a bacterial pathogen known for causing respiratory disease in poultry [9], and Riemerella anatipestifer which causes ‘‘duckling disease’’ in waterfowl and turkeys [10,11]. The genus Capnocytophaga includes seven species found in normal human oral flora and C. canimorsus found in the normal flora of dogs and cats. We show that a surface-localized sialidase plays a key role in initiating an extensive deglycosylation process of host cell glycan structures and that this feeding mechanism serves as a basis for growth and persistence of C. canimorsus in vivo
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