Bactericidal Permeability-Increasing Proteins Shape Host-Microbe Interactions.

David A Relman,Sabrina Koehler,Benjamin C Krasity,Edward G Ruby,Margaret J Mcfall-Ngai,Fangmin Chen,Suzanne M Peyer,Xiaoping Zhang

doi:10.1128/mbio.00040-17

Abstract

ABSTRACTWe characterized bactericidal permeability-increasing proteins (BPIs) of the squid Euprymna scolopes, EsBPI2 and EsBPI4. They have molecular characteristics typical of other animal BPIs, are closely related to one another, and nest phylogenetically among invertebrate BPIs. Purified EsBPIs had antimicrobial activity against the squid’s symbiont, Vibrio fischeri, which colonizes light organ crypt epithelia. Activity of both proteins was abrogated by heat treatment and coincubation with specific antibodies. Pretreatment under acidic conditions similar to those during symbiosis initiation rendered V. fischeri more resistant to the antimicrobial activity of the proteins. Immunocytochemistry localized EsBPIs to the symbiotic organ and other epithelial surfaces interacting with ambient seawater. The proteins differed in intracellular distribution. Further, whereas EsBPI4 was restricted to epithelia, EsBPI2 also occurred in blood and in a transient juvenile organ that mediates hatching. The data provide evidence that these BPIs play different defensive roles early in the life of E. scolopes, modulating interactions with the symbiont.

Highlights

We characterized bactericidal permeability-increasing proteins (BPIs) of the squid Euprymna scolopes, EsBPI2 and EsBPI4
The two BPIs characterized in this study, EsBPI2 and EsBPI4, exhibit typical biochemical, structural, and antimicrobial characteristics of animal BPIs
They are similar to the BPIs that are secreted along mucosal surfaces in terrestrial vertebrates, such as birds [5] and mammals [18]. The presence of both EsBPI2 and EsBPI4 in the epithelia of the juvenile light organ (Fig. 4C to F and N to Q) suggests roles for these proteins in specificity and control of symbiont populations. These proteins colocalize with other antimicrobials, such as nitric oxide [19], EsPGRP2 (E. scolopes peptidoglycan recognition protein 2) [20], galaxin [21], and hemocyanin [22] that are secreted with low-pH mucous stores from the superficial ciliated fields of the light organ within minutes following hatching

Summary

Introduction

We characterized bactericidal permeability-increasing proteins (BPIs) of the squid Euprymna scolopes, EsBPI2 and EsBPI4 They have molecular characteristics typical of other animal BPIs, are closely related to one another, and nest phylogenetically among invertebrate BPIs. Purified EsBPIs had antimicrobial activity against the squid’s symbiont, Vibrio fischeri, which colonizes light organ crypt epithelia. LBP typically presents LPS to host surface receptors, an activity that induces changes in host gene expression; in contrast, the BPIs are bactericidal, binding to the surface and compromising the integrity of the bacterial cell envelope These two functionally distinct classes of proteins are in the same family and share a characteristic molecular architecture, they have diverged considerably over evolution; even the isoforms of BPIs within a single species typically have a sequence similarity of only 40 to 50% [1, 4, 5]. This body plan demands robust mechanisms to prevent uncontrolled colonization of these surfaces by bacterioplankton

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Conclusion