Abstract
Photorhabdus asymbiotica is one of the three recognized species of the Photorhabdus genus, which consists of gram-negative bioluminescent bacteria belonging to the family Morganellaceae. These bacteria live in a symbiotic relationship with nematodes from the genus Heterorhabditis, together forming a complex that is highly pathogenic for insects. Unlike other Photorhabdus species, which are strictly entomopathogenic, P. asymbiotica is unique in its ability to act as an emerging human pathogen. Analysis of the P. asymbiotica genome identified a novel fucose-binding lectin designated PHL with a strong sequence similarity to the recently described P. luminescens lectin PLL. Recombinant PHL exhibited high affinity for fucosylated carbohydrates and the unusual disaccharide 3,6-O-Me2-Glcβ1–4(2,3-O-Me2)Rhaα-O-(p-C6H4)-OCH2CH2NH2 from Mycobacterium leprae. Based on its crystal structure, PHL forms a seven-bladed β-propeller assembling into a homo-dimer with an inter-subunit disulfide bridge. Investigating complexes with different ligands revealed the existence of two sets of binding sites per monomer—the first type prefers l-fucose and its derivatives, whereas the second type can bind d-galactose. Based on the sequence analysis, PHL could contain up to twelve binding sites per monomer. PHL was shown to interact with all types of red blood cells and insect haemocytes. Interestingly, PHL inhibited the production of reactive oxygen species induced by zymosan A in human blood and antimicrobial activity both in human blood, serum and insect haemolymph. Concurrently, PHL increased the constitutive level of oxidants in the blood and induced melanisation in haemolymph. Our results suggest that PHL might play a crucial role in the interaction of P. asymbiotica with both human and insect hosts.
Highlights
Photorhabdus is a genus of three species belonging to the gram-negative entomopathogenic bacteria of the family Morganellaceae
We focused on the lectin identified in P. asymbiotica genome that may be crucial for the early stage of infection
We investigated influence of PHL on immune system of human and insect to propose the biological role for this lectin
Summary
Photorhabdus is a genus of three species belonging to the gram-negative entomopathogenic bacteria of the family Morganellaceae. Unlike the other two species of the genus, P. asymbiotica is an insect pathogen. Using a still poorly understood mechanism, P. asymbiotica can infect humans and cause both locally invasive soft tissue infection and disseminated bacteraemic disease characterised by multifocal skin and soft tissue abscesses [1,2,3,4]. While other members of the genus are not able to replicate and survive above 32–34 ̊C, P. asymbiotica has the ability to grow at temperatures above 37 ̊C [4,5,6]. P. asymbiotica can be further subdivided into two apparent subspecies—American and Australian isolates according to genotypic criteria and the occurrence of human infection. It was found that Australian strains are more virulent than American ones [3,7,8]
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