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House spider genome uncovers evolutionary shifts in the diversity and expression of black widow venom proteins associated with extreme toxicity.

ABSTRACT: Black widow spiders are infamous for their neurotoxic venom, which can cause extreme and long-lasting pain. This unusual venom is dominated by latrotoxins and latrodectins, two protein families virtually unknown outside of the black widow genus Latrodectus, that are difficult to study given the paucity of spider genomes. Using tissue-, sex- and stage-specific expression data, we analyzed the recently sequenced genome of the house spider (Parasteatoda tepidariorum), a close relative of black widows, to investigate latrotoxin and latrodectin diversity, expression and evolution.We discovered at least 47 latrotoxin genes in the house spider genome, many of which are tandem-arrayed. Latrotoxins vary extensively in predicted structural domains and expression, implying their significant functional diversification. Phylogenetic analyses show latrotoxins have substantially duplicated after the Latrodectus/Parasteatoda split and that they are also related to proteins found in endosymbiotic bacteria. Latrodectin genes are less numerous than latrotoxins, but analyses show their recruitment for venom function from neuropeptide hormone genes following duplication, inversion and domain truncation. While latrodectins and other peptides are highly expressed in house spider and black widow venom glands, latrotoxins account for a far smaller percentage of house spider venom gland expression.The house spider genome sequence provides novel insights into the evolution of venom toxins once considered unique to black widows. Our results greatly expand the size of the latrotoxin gene family, reinforce its narrow phylogenetic distribution, and provide additional evidence for the lateral transfer of latrotoxins between spiders and bacterial endosymbionts. Moreover, we strengthen the evidence for the evolution of latrodectin venom genes from the ecdysozoan Ion Transport Peptide (ITP)/Crustacean Hyperglycemic Hormone (CHH) neuropeptide superfamily. The lower expression of latrotoxins in house spiders relative to black widows, along with the absence of a vertebrate-targeting ?-latrotoxin gene in the house spider genome, may account for the extreme potency of black widow venom.

SUBMITTER: Gendreau KL

PROVIDER: S-EPMC5314461 | biostudies-literature | 2017 Feb

REPOSITORIES: biostudies-literature

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House spider genome uncovers evolutionary shifts in the diversity and expression of black widow venom proteins associated with extreme toxicity.

Gendreau Kerry L KL Haney Robert A RA Schwager Evelyn E EE Wierschin Torsten T Stanke Mario M Richards Stephen S Garb Jessica E JE

BMC genomics 20170216 1

<h4>Background</h4>Black widow spiders are infamous for their neurotoxic venom, which can cause extreme and long-lasting pain. This unusual venom is dominated by latrotoxins and latrodectins, two protein families virtually unknown outside of the black widow genus Latrodectus, that are difficult to study given the paucity of spider genomes. Using tissue-, sex- and stage-specific expression data, we analyzed the recently sequenced genome of the house spider (Parasteatoda tepidariorum), a close rel ...[more]

PMID: 28209133

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Project description:Spiders use their venom for defence and to capture prey. These venoms contain a cocktail of biologically active compounds that display several different biological activities, such as large molecules and small molecules including peptides, proteins/enzymes, and other components. Thus, venom constituents have attracted the attention of biochemists and pharmacologists over the years. The brown widow spider (Latrodectus geometricus) is a venomous spider found worldwide, including in Thailand. This spider causes human injuries, and the venom has many potential applications. In this study, we investigated the complexity and pharmacology of brown widow spider venom. Spider crude venom was investigated using partial proteome techniques and enzymatic activity, toxicity, and antibacterial activity assessments. We found that crude venom displayed a wide range of molecular masses from 19 to over 97 kDa, with molecular masses of 66 kDa intensely stained. Peptides and proteins were identified by liquid chromatography-mass spectrometry/mass spectrometry (LC-MS/MS), which showed that the crude venom contained a variety of substances, including latrotoxins, apolipophorins, hemocyanins, chitinases, arginine kinase, allergen antigen 5-like protein, astacin-like metalloproteases, and serine proteases. High hyaluronidase activity was observed based on the turbidimetric method. The venom presented toxicity in crickets (PD50 = 0.73 ± 0.10 ?g/g body weight), and substantial envenomation symptoms, such as slow-motion movement, paralysis, and even death, were noted. Moreover, this venom exhibited potential antibacterial activity against the gram-positive Bacillus subtilis but not the gram-negative Pseudomonas aeruginosa. Spider venom contains numerous molecules with biological activity, such as latrotoxins, which affect insects, and enzymes. In addition to latrotoxins, certain enzymes in venom are hypothesized to exhibit toxicity and antimicrobial activity. This study provides important information for the further development of natural compounds or insecticidal toxins.

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House spider genome uncovers evolutionary shifts in the diversity and expression of black widow venom proteins associated with extreme toxicity.

Publications

House spider genome uncovers evolutionary shifts in the diversity and expression of black widow venom proteins associated with extreme toxicity.

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