Ticks Resist Skin Commensals with Immune Factor of Bacterial Origin

Hayes, Beth M.; Radkov, Atanas; Yarza, Fauna; Flores, Sebastián; Kim, Rachel; Zhao, Ziyi; Lexa, Katrina W.; Marnin, Liron; Biboy, Jacob; Bowcut, Victoria; Vollmer, Waldemar; Pedra, Joao H. F.; Chou, Seemay

doi:10.1016/j.cell.2020.10.042

Cited by 33 publications

(24 citation statements)

References 63 publications

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“…The majority of studies on prokaryote-to-insect HGT events have discovered genes involved in conferring new metabolic capabilities, particularly those that allow insects to colonize new plant hosts and adapt to existing ones ( Daimon et al 2008 ; Wybouw et al 2016 ), or toxin-encoding genes involved in antibacterial defenses ( Di Lelio et al 2019 ; Hayes et al 2020 ; Li et al 2021 ). However, our study highlights that HGT of a new functional class of proteins, toxins that antagonize eukaryotic cells, may be more common among insects than previously known.…”

Section: Discussionmentioning

confidence: 99%

“…HGT facilitates the evolution of novelty in animal immune systems, particularly among arthropods. Antibacterial toxins transferred from bacteria have been described in Ixodes ticks and in several species of Coccinellinae ladybird beetles ( Hayes et al 2020 ; Li et al 2021 ). Some horizontally transferred genes (HTGs) have been co-opted as effectors of the insect immune system.…”

Section: Introductionmentioning

confidence: 99%

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Horizontal Transfer of Microbial Toxin Genes to Gall Midge Genomes

Verster

Tarnopol

Akalu

et al. 2021

Genome Biology and Evolution

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A growing body of evidence has underscored the role of horizontal gene transfer (HGT) in animal evolution. Previously, we discovered the horizontal transfer of the gene encoding the eukaryotic genotoxin cytolethal distending toxin B (cdtB) from the pea aphid Acyrthosiphon pisum secondary endosymbiont (APSE) phages to drosophilid and aphid nuclear genomes. Here, we report cdtB in the nuclear genome of the gall-forming ‘swede midge’ Contarinia nasturtii (Diptera: Cecidomyiidae) via HGT. We searched all available gall midge genome sequences for evidence of APSE-to-insect HGT events and found five toxin genes (aip56, cdtB, lysozyme, rhs, and sltxB) transferred horizontally to cecidomyiid nuclear genomes. Surprisingly, phylogenetic analyses of HGT candidates indicated APSE phages were often not the ancestral donor lineage of the toxin gene to cecidomyiids. We used a phylogenetic signal statistic to test a transfer-by-proximity hypothesis for animal HGT, which suggested that microbe-to-insect HGT was more likely between taxa that share environments than those from different environments. Many of the toxins we found in midge genomes target eukaryotic cells, and catalytic residues important for toxin function are conserved in insect copies. This class of horizontally transferred, eukaryotic cell-targeting genes is potentially important in insect adaptation.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Horizontal Transfer of Microbial Toxin Genes to Gall Midge Genomes

Verster

Tarnopol

Akalu

et al. 2021

Genome Biology and Evolution

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“…Possible explanations for this exclusivity include: a) descent with modification from a shared ancestral protein sequence present before the divergence of Metastriate and Prostriate lineages, b) descent from independent ancestral protein sequences with loss of a class [i.e. "gene death" (Nei and Rooney, 2005)] following Metastriate/Prostriate divergence, or c) origin by horizontal gene transfer from another organisma phenomenon that has been shown to occur in arthropod lineages and has functional importance at the tick host interface (Chou et al, 2015;Hayes et al, 2020). These alternative scenarios may be resolved by further analysis of ticks from different lineages.…”

Section: Discussionmentioning

confidence: 99%

Phylogenetic Analysis Indicates That Evasin-Like Proteins of Ixodid Ticks Fall Into Three Distinct Classes

Bhattacharya

Nuttall

2021

Front. Cell. Infect. Microbiol.

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Chemokines are structurally related proteins that activate leucocyte migration in response to injury or infection. Tick saliva contains chemokine-binding proteins or evasins which likely neutralize host chemokine function and inflammation. Biochemical characterisation of 50 evasins from Ixodes, Amblyomma and Rhipicephalus shows that they fall into two functional classes, A and B, with exclusive binding to either CC- or CXC- chemokines, respectively. Class A evasins, EVA1 and EVA4 have a four-disulfide-bonded core, whereas the class B evasin EVA3 has a three-disulfide-bonded “knottin” structure. All 29 class B evasins have six cysteine residues conserved with EVA3, arrangement of which defines a Cys6-motif. Nineteen of 21 class A evasins have eight cysteine residues conserved with EVA1/EVA4, the arrangement of which defines a Cys8-motif. Two class A evasins from Ixodes (IRI01, IHO01) have less than eight cysteines. Many evasin-like proteins have been identified in tick salivary transcriptomes, but their phylogenetic relationship with respect to biochemically characterized evasins is not clear. Here, using BLAST searches of tick transcriptomes with biochemically characterized evasins, we identify 292 class A and 157 class B evasins and evasin-like proteins from Prostriate (Ixodes), and Metastriate (Amblyomma, Dermacentor, Hyalomma, Rhipicephalus) ticks. Phylogenetic analysis shows that class A evasins/evasin-like proteins segregate into two classes, A1 and A2. Class A1 members are exclusive to Metastriate ticks and typically have a Cys8-motif and include EVA1 and EVA4. Class A2 members are exclusive to Prostriate ticks, lack the Cys8-motif, and include IHO01 and IRI01. Class B evasins/evasin-like proteins are present in both Prostriate and Metastriate lineages, typically have a Cys6-motif, and include EVA3. Most evasins/evasin-like proteins in Metastriate ticks belong to class A1, whereas in Prostriate species they are predominantly class B. In keeping with this, the majority of biochemically characterized Metastriate evasins bind CC-chemokines, whereas the majority of Prostriate evasins bind CXC-chemokines. While the origin of the structurally dissimilar classes A1 and A2 is yet unresolved, these results suggest that class B evasin-like proteins arose before the divergence of Prostriate and Metastriate lineages and likely functioned to neutralize CXC-chemokines and support blood feeding.

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“…Indeed, it was recently shown that Dae2 is physically unable to overcome the outer membrane structure of the outer membrane of Gramnegative bacteria; thus, it does not present lytic activity against B. burgdorferi, suggesting the need for other factors, such as membrane-permeabilizing agents (100). As Dae2 is delivered to the vertebrate host bite site via saliva and exhibits strong activity against bacteria usually encountered in the host skin, this AMP may protect ticks from the acquisition and proliferation of host skin microbes (100).…”

Section: Antimicrobial Peptides: May the "Source" Be With You!mentioning

confidence: 99%

Tick Immune System: What Is Known, the Interconnections, the Gaps, and the Challenges

et al. 2021

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Ticks are ectoparasitic arthropods that necessarily feed on the blood of their vertebrate hosts. The success of blood acquisition depends on the pharmacological properties of tick saliva, which is injected into the host during tick feeding. Saliva is also used as a vehicle by several types of pathogens to be transmitted to the host, making ticks versatile vectors of several diseases for humans and other animals. When a tick feeds on an infected host, the pathogen reaches the gut of the tick and must migrate to its salivary glands via hemolymph to be successfully transmitted to a subsequent host during the next stage of feeding. In addition, some pathogens can colonize the ovaries of the tick and be transovarially transmitted to progeny. The tick immune system, as well as the immune system of other invertebrates, is more rudimentary than the immune system of vertebrates, presenting only innate immune responses. Although simpler, the large number of tick species evidences the efficiency of their immune system. The factors of their immune system act in each tick organ that interacts with pathogens; therefore, these factors are potential targets for the development of new strategies for the control of ticks and tick-borne diseases. The objective of this review is to present the prevailing knowledge on the tick immune system and to discuss the challenges of studying tick immunity, especially regarding the gaps and interconnections. To this end, we use a comparative approach of the tick immune system with the immune system of other invertebrates, focusing on various components of humoral and cellular immunity, such as signaling pathways, antimicrobial peptides, redox metabolism, complement-like molecules and regulated cell death. In addition, the role of tick microbiota in vector competence is also discussed.

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Ticks Resist Skin Commensals with Immune Factor of Bacterial Origin

Cited by 33 publications

References 63 publications

Horizontal Transfer of Microbial Toxin Genes to Gall Midge Genomes

Horizontal Transfer of Microbial Toxin Genes to Gall Midge Genomes

Phylogenetic Analysis Indicates That Evasin-Like Proteins of Ixodid Ticks Fall Into Three Distinct Classes

Tick Immune System: What Is Known, the Interconnections, the Gaps, and the Challenges

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