Polydnavirus
Encyclopedia
The Polydnaviruses (PDV) are a family of insect virus
es that contain two genera
: Ichnoviruses (IV) and Bracoviruses (BV). The ichnoviruses occur in ichneumonid wasps
species and bracoviruses in braconid wasps
. The genome
of the virus is composed of multiple segments of double-stranded, superhelical DNA packaged in capsid proteins and a double layer (IV) or single layer (BV) envelope. Little or no sequence homology exists between BV and IV, suggesting that the two genera evolved independently.
These viruses are part of a unique biological system consisting of an endoparasitic wasp (parasitoid
), an insect (usually lepidoptera
n) larva, and the virus. The full genome
of the virus is integrated into the genome of the wasp and the virus only replicates in specific cells in the female wasp's reproductive system. The virus is injected along with the wasp egg into the body cavity of a lepidopteran host caterpillar and infects cells of the caterpillar. The infection does not lead to replication of new viruses, rather it affects the caterpillar's immune system
. Without the virus infection, phagocytic
hemocyte
s (blood cells) will encapsulate and kill the wasp egg but the immune suppression caused by the virus allows for survival of the wasp egg, leading to hatching and complete development of the immature wasp in the caterpillar. Additionally, genes expressed from the polydnavirus in the parasitised host alter host development and metabolism to be beneficial for the growth and survival of the parasitoid larva. Thus the virus and wasp have a symbiotic (mutualistic) relationship.
However, the morphology of the two genera are different when observed by electron microscopy. Ichnoviruses tend to be ovoid (egg-shaped) while bracoviruses are short rods.
analysis suggests a very long association of the viruses with the wasps (greater than 70 million years).
Two proposals have been advanced for how the wasp/virus association developed. The first suggests that the virus is derived from wasp genes. Many parasitoids that do not use PDVs inject proteins that provide many of the same functions, that is, a suppression of the immune response to the parasite egg. In this model, the braconid and ichneumonid wasps packaged genes for these functions into the viruses – essentially creating a gene-transfer system that results in the caterpillar producing the immune-suppressing factors. In this scenario, the PDV structural proteins (capsids) were probably "borrowed" from existing viruses.
The alternative proposal suggests that ancestral wasps developed a beneficial association with an existing virus that eventually led to the integration of the virus into the wasp’s genome. Following integration, the genes responsible for virus replication and the capsids were (eventually) no longer included in the PDV genome. This hypothesis is supported by the distinct morphology differences between IV and BV, suggesting different ancestral viruses for the two families. The IV have remarkable similarities to ascovirus
es while BV may be related to baculovirus
es
The family Polydnaviridae may have evolved from the Ascoviridae.
When a big body (wasp eggs or experimentally, small particles) is introduced into an insect's body, the classic immune reaction is the encapsulation by the hematocytes. An encapsuled body can also be melanised in order to asphyxiate it, thanks to another type of hemocyte, which uses the Phenoloxydase enzyme to produce melanin. Little particles can be phagocyted, and macrophage cells can then be also melanised in a nodule. Finally, insects can also have a humoral immunity, with production of antiviral peptids.(1)
PolyDNAvirus protect the Hymenoptera larvae from the host immune system, acting at different levels.
* First they can disable or destroy hematocytes. The polyDNAvirus associated with Cotesia rubecula, code for un protein CrV1 that desorganise actin filaments in hematocytes, so those cells become less able to move and adher to the larvae (1). Microplitis demolitor Bracovirus (MdBV) induce apoptosis of hematocytes, thanks to its gene PTP-H2 (1). It also decreases hematocytes' capacity of adhesion, thanks to its gene Glc1.8. The gene also decrease phagocytosis.(2)
* PolyDNAvirus can also act on melanisation, MdBV interfer with the production of Phenoloxydase Enzyme.(3)
* Finally, polyDNAvirus can also produce viral Ankyris, that interfere with production of antiviral peptids.(4) Some Ichnovirus,
Vankyrin can also prevent apoptosis, the extrem reaction of a cell to block viral propagation.(5)
VLPs are very close to viruses in their structure but they don't carry any nucleic acid.
For example, Venturia canescens (Ichneumonidea) and Leptopilina sp. (Figitidaea) produc VLPs.
VLPs can be compared to PolyDNAvirus because they are secreted in the same way, and they both act to protect the larvae against the host's immune system. V. canescens-VLPs (VcVLP1, VcVLP2,VcNEP …) are produced in the calix cells before they go to the oviducts. But they are composed of proteins that are closer in structure and function to Hymenoptera's proteins than to viral proteins. This suggests that they don't have a viral origin, unlike polyDNAvirus.
VLPs protect the Hymenoptera larvae locally, whereas polyDNAvirus can have a more global effect. VLPs allow the larvae to escape the immune system: the larva is not recognised as harmful by its host, or the immune cells can't interact with it thanks to the VLPs.(6)
The wasp Leptopilina heterotoma secrete VLPs that are able to penetrate into the Lamellocytes, thanks to specific receptors, and then modify their shape and surface properties so they become inefficient and the larvae is safe from encapsulation.(7)
It is interesting to consider the microRNA phenomenon in the polyDNAvirus context. Lots of hypotheses can be formulated :
Virus
A virus is a small infectious agent that can replicate only inside the living cells of organisms. Viruses infect all types of organisms, from animals and plants to bacteria and archaea...
es that contain two genera
Genera
Genera is a commercial operating system and development environment for Lisp machines developed by Symbolics. It is essentially a fork of an earlier operating system originating on the MIT AI Lab's Lisp machines which Symbolics had used in common with LMI and Texas Instruments...
: Ichnoviruses (IV) and Bracoviruses (BV). The ichnoviruses occur in ichneumonid wasps
Ichneumonidae
Ichneumonidae is a family within the insect order Hymenoptera. Insects in this family are commonly called ichneumon wasps. Less exact terms are ichneumon flies , or scorpion wasps due to the extreme lengthening and curving of the abdomen...
species and bracoviruses in braconid wasps
Braconidae
Braconidae is a family of parasitoid wasps and one of the richest families of insects. Between 50,000 and 150,000 species exist worldwide. The species are grouped into about 45 subfamilies and 1,000 genera, some important ones being: Ademon, Aphanta, Asobara, Bracon hebetor, Cenocoelius, Chaenusa,...
. The genome
Genome
In modern molecular biology and genetics, the genome is the entirety of an organism's hereditary information. It is encoded either in DNA or, for many types of virus, in RNA. The genome includes both the genes and the non-coding sequences of the DNA/RNA....
of the virus is composed of multiple segments of double-stranded, superhelical DNA packaged in capsid proteins and a double layer (IV) or single layer (BV) envelope. Little or no sequence homology exists between BV and IV, suggesting that the two genera evolved independently.
Biology
Parasitoid
A parasitoid is an organism that spends a significant portion of its life history attached to or within a single host organism in a relationship that is in essence parasitic; unlike a true parasite, however, it ultimately sterilises or kills, and sometimes consumes, the host...
), an insect (usually lepidoptera
Lepidoptera
Lepidoptera is a large order of insects that includes moths and butterflies . It is one of the most widespread and widely recognizable insect orders in the world, encompassing moths and the three superfamilies of butterflies, skipper butterflies, and moth-butterflies...
n) larva, and the virus. The full genome
Genome
In modern molecular biology and genetics, the genome is the entirety of an organism's hereditary information. It is encoded either in DNA or, for many types of virus, in RNA. The genome includes both the genes and the non-coding sequences of the DNA/RNA....
of the virus is integrated into the genome of the wasp and the virus only replicates in specific cells in the female wasp's reproductive system. The virus is injected along with the wasp egg into the body cavity of a lepidopteran host caterpillar and infects cells of the caterpillar. The infection does not lead to replication of new viruses, rather it affects the caterpillar's immune system
Immune system
An immune system is a system of biological structures and processes within an organism that protects against disease by identifying and killing pathogens and tumor cells. It detects a wide variety of agents, from viruses to parasitic worms, and needs to distinguish them from the organism's own...
. Without the virus infection, phagocytic
Phagocyte
Phagocytes are the white blood cells that protect the body by ingesting harmful foreign particles, bacteria, and dead or dying cells. Their name comes from the Greek phagein, "to eat" or "devour", and "-cyte", the suffix in biology denoting "cell", from the Greek kutos, "hollow vessel". They are...
hemocyte
Hemocyte
A hemocyte is a cell that plays a role in the immune system of invertebrates. It is found within the hemolymph.Hemocytes are phagocytes of invertebrates....
s (blood cells) will encapsulate and kill the wasp egg but the immune suppression caused by the virus allows for survival of the wasp egg, leading to hatching and complete development of the immature wasp in the caterpillar. Additionally, genes expressed from the polydnavirus in the parasitised host alter host development and metabolism to be beneficial for the growth and survival of the parasitoid larva. Thus the virus and wasp have a symbiotic (mutualistic) relationship.
Characteristics
Both genera of PDV share certain characteristics:- the virus particles of each contain multiple segments of dsDNA with each segment containing only part of the full genome (much like chromosomes in eukaryotic organisms);
- the genome of each is integrated into the host wasp genome;
- the virus particles are only replicated (produced) in specific cell types in the female wasp's reproductive organs.
However, the morphology of the two genera are different when observed by electron microscopy. Ichnoviruses tend to be ovoid (egg-shaped) while bracoviruses are short rods.
Evolution
Nucleic acidNucleic acid
Nucleic acids are biological molecules essential for life, and include DNA and RNA . Together with proteins, nucleic acids make up the most important macromolecules; each is found in abundance in all living things, where they function in encoding, transmitting and expressing genetic information...
analysis suggests a very long association of the viruses with the wasps (greater than 70 million years).
Two proposals have been advanced for how the wasp/virus association developed. The first suggests that the virus is derived from wasp genes. Many parasitoids that do not use PDVs inject proteins that provide many of the same functions, that is, a suppression of the immune response to the parasite egg. In this model, the braconid and ichneumonid wasps packaged genes for these functions into the viruses – essentially creating a gene-transfer system that results in the caterpillar producing the immune-suppressing factors. In this scenario, the PDV structural proteins (capsids) were probably "borrowed" from existing viruses.
The alternative proposal suggests that ancestral wasps developed a beneficial association with an existing virus that eventually led to the integration of the virus into the wasp’s genome. Following integration, the genes responsible for virus replication and the capsids were (eventually) no longer included in the PDV genome. This hypothesis is supported by the distinct morphology differences between IV and BV, suggesting different ancestral viruses for the two families. The IV have remarkable similarities to ascovirus
Ascovirus
Ascovirus is a family of double strand DNA viruses that infect primarily invertebrates. Currently only a single genus in this family is recognised: Ascovirus....
es while BV may be related to baculovirus
Baculovirus
The baculoviruses are a family of large rod-shaped viruses that can be divided to two genera: nucleopolyhedroviruses and granuloviruses . While GVs contain only one nucleocapsid per envelope, NPVs contain either single or multiple nucleocapsids per envelope. The enveloped virions are further...
es
The family Polydnaviridae may have evolved from the Ascoviridae.
Effect on host immunity
An insects immunity is composed of several mechanisms and all of them can be triggered in the host when the wasp lays its eggs, and during the larvae development.When a big body (wasp eggs or experimentally, small particles) is introduced into an insect's body, the classic immune reaction is the encapsulation by the hematocytes. An encapsuled body can also be melanised in order to asphyxiate it, thanks to another type of hemocyte, which uses the Phenoloxydase enzyme to produce melanin. Little particles can be phagocyted, and macrophage cells can then be also melanised in a nodule. Finally, insects can also have a humoral immunity, with production of antiviral peptids.(1)
PolyDNAvirus protect the Hymenoptera larvae from the host immune system, acting at different levels.
* First they can disable or destroy hematocytes. The polyDNAvirus associated with Cotesia rubecula, code for un protein CrV1 that desorganise actin filaments in hematocytes, so those cells become less able to move and adher to the larvae (1). Microplitis demolitor Bracovirus (MdBV) induce apoptosis of hematocytes, thanks to its gene PTP-H2 (1). It also decreases hematocytes' capacity of adhesion, thanks to its gene Glc1.8. The gene also decrease phagocytosis.(2)
* PolyDNAvirus can also act on melanisation, MdBV interfer with the production of Phenoloxydase Enzyme.(3)
* Finally, polyDNAvirus can also produce viral Ankyris, that interfere with production of antiviral peptids.(4) Some Ichnovirus,
Vankyrin can also prevent apoptosis, the extrem reaction of a cell to block viral propagation.(5)
Virus like particles
Another strategy used by parasitoïd Hymenoptera to protect their offspring is production of Virus Like Particles.VLPs are very close to viruses in their structure but they don't carry any nucleic acid.
For example, Venturia canescens (Ichneumonidea) and Leptopilina sp. (Figitidaea) produc VLPs.
VLPs can be compared to PolyDNAvirus because they are secreted in the same way, and they both act to protect the larvae against the host's immune system. V. canescens-VLPs (VcVLP1, VcVLP2,VcNEP …) are produced in the calix cells before they go to the oviducts. But they are composed of proteins that are closer in structure and function to Hymenoptera's proteins than to viral proteins. This suggests that they don't have a viral origin, unlike polyDNAvirus.
VLPs protect the Hymenoptera larvae locally, whereas polyDNAvirus can have a more global effect. VLPs allow the larvae to escape the immune system: the larva is not recognised as harmful by its host, or the immune cells can't interact with it thanks to the VLPs.(6)
The wasp Leptopilina heterotoma secrete VLPs that are able to penetrate into the Lamellocytes, thanks to specific receptors, and then modify their shape and surface properties so they become inefficient and the larvae is safe from encapsulation.(7)
Micro-RNA
MicroRNA are small RNA produced in the host cells thanks to a specific enzymatic machinery. They allows viral RNA destruction. MicroRNA hang on viral-RNA because they are complementary. Then the complex is recognised by an enzyme that destroys it. This phenomenon is known as PTGS (for post transcriptional gene silencing)(8)It is interesting to consider the microRNA phenomenon in the polyDNAvirus context. Lots of hypotheses can be formulated :
- Braconidae carry nudivirus-related genes in their genome (9), so they are may be able to produce microRNA against nudivirus, as an innate immunity.
- Wasps perhaps use microRNA to contrôl the viral genes they carry.
- PolyDNAvirus can also use PTGS to interfere with the host's gene expression.
- PTGS is also used for organisms' development, using the same enzymes as antiviral gene silencing, so we can imagine that if the host use PTGS against polyDNAvirus, perhaps it also affects its development.
External links
- http://research.biology.arizona.edu/mosquito/willott/507/polydnaviruses.html
- Polydnavirus DNA is Integrated in the DNA of Its Parasitoid Wasp Host - article from the Proceedings of the National Academy of SciencesProceedings of the National Academy of SciencesThe Proceedings of the National Academy of Sciences of the United States of America, usually referred to as PNAS, is the official journal of the United States National Academy of Sciences...
.- Abstract of the PNAS article.
- Genome Sequence of a Polydnavirus: Insights into Symbiotic Virus Evolution article from Science.
- Viralzone: Polydnaviridae