Natural invertebrate hosts of iridoviruses (Iridoviridae)

Hospederos naturales de los iridovirus de invertebrados

FORUM

Natural invertebrate hosts of iridoviruses (Iridoviridae)

Hospederos naturales de los iridovirus de invertebrados

Trevor Williams

Instituto de Ecología A.C., Xalapa 91070, Veracruz, Mexico; [e-mail]

ABSTRACT

Invertebrate iridescent viruses (IIVs) are icosahedral DNA viruses that infect invertebrates, mainly insects and terrestrial isopods, in damp and aquatic habitats. Exhaustive searches of databases resulted in the identification of 79 articles reporting 108 invertebrate species naturally infected by confirmed or putative iridoviruses. Of these, 103 (95%) were arthropods and the remainder were molluscs, an annelid worm and a nematode. Nine species were from marine habitats. Of the 99 non-marine species, 49 were from terrestrial habitats and 50 were aquatic, especially the aquatic stages of Diptera (44 species). The abundance of records from species of Aedes,Ochlerotatus and Psorophora contrasts markedly with a paucity of records from species of Anopheles,Culex and Culiseta. Records from terrestrial isopods are numerous (19 species), although the diversity of IIVs that infect them is mostly unstudied. IIV infections have been reported from every continent, except Antarctica, but there are few records from Africa, southern Asia and Latin America. Most reports describe patent IIV infections as rare whereas inapparent (covert) infection may be common in certain species. The relationship between particle size and iridescent colour of the host is found to be consistent with optical theory in the great majority of cases. Only 24 reported IIVs from insect hosts have partial characterization data and only two have been subjected to complete genome sequencing. I show that the rate of publication on IIVs has slowed from 1990 to the present, and I draw a number of conclusions and suggestions from the host list and make recommendations for future research efforts.

Key words: Infection, natural host, location, particle size, prevalence, virus characterization data

RESUMEN

Los virus iridiscentes de invertebrados (VIIs) son virus icosaedrales de ADN que infectan a invertebrados, principalmente insectos e isópodos terrestres en hábitats húmedos y acuáticos. Búsquedas extensivas de bases de datos resultaron en la identificación de 79 artículos científicos, los cuales reportaron 108 especies de invertebrados infectados naturalmente por iridovirus. De estos, 103 (95%) fueron artrópodos y los otros fueron moluscos, un anélido y un nematodo. Nueve especies fueron de hábitats marinos. De las 99 especies no marinas, 49 fueron terrestres y 50 fueron acuáticas, especialmente los estadios acuáticos de dípteros (44 especies). La abundancia de infecciones en especies de Aedes,Ochlerotatus y Psorophora se contrasta marcadamente con la escasez de casos en especies de Anopheles,Culex y Culiseta. Reportes de infecciones de los isópodos terrestres son numerosos (19 especies), aunque la diversidad de los VII que los infectan es desconocida. Se han reportado infecciones por VIIs de todos los continentes, excepto Antártica, pero se notan pocos ejemplos de África, Asia y Latinoamérica. La mayoría de los artículos señala que las infecciones patentes son poco comunes, mientras que las infecciones enmascaradas (subletales) pueden ser comunes en algunas especies. La relación entre el tamaño de la partícula y el color iridiscente concuerda con la teoría óptica en casi todos los casos. Veinticuatro de los VIIs de insectos han sido caracterizados parcialmente y solo dos de éstos han sido secuenciados completamente. Demuestro que el ritmo de publicación sobre los VIIs ha disminuido en los últimos 15 años, señalo varias conclusiones y sugerencias de la lista de especies de huéspedes y presento algunas recomendaciones para la investigación futura con este grupo de patógenos.

Palabras Clave: Abundancia, infección, huésped natural, tamaño de partícula, caracterización de virus

Iridoviruses are icosahedral particles that contain a double stranded DNA genome, and are assigned to one of five genera in the family Iridoviridae (Chinchar et al. 2005). Members of Ranavirus,Lymphocystivirus and Megalocytivirus infect cold-blooded vertebrates, particularly fish, amphibians and reptiles. In contrast, members of Iridovirus and Chloriridovirus infect invertebrates, mainly insects and terrestrial isopods, in damp and aquatic habitats, and are both known as invertebrate iridescent viruses (IIVs) because of the opalescent hues observed in heavily infected hosts. Such patent infections are almost invariably lethal, but there is now growing evidence that covert sublethal infections can be common in certain host species (Williams 1993, Tonka & Weiser 2000). Such covertly infected hosts can survive to the adult stage and reproduce, although covert infection is associated with extended development time, reduced adult body size and reduced fecundity and longevity (Marina et al. 1999, 2003).

Despite records of IIV infections from agriculturally and medically important species of insects, these viruses are considered to have little potential as agents of biological control due to the often low prevalence of patent disease and the broad host range displayed in laboratory tests (Ohba 1975, Henderson et al. 2001, Jakob et al. 2002). This has led to a lack of interest in the study of these viruses and a resulting paucity of information concerning their biology and survival in invertebrate populations. Indeed, the mechanisms of transmission of most IIVs remain unclear, although cannibalism and wounding have been shown to be viable mechanisms in some species (Carter 1973, Grosholz 1992, Undeen & Fukuda 1994, Marina et al. 2005, Williams & Hernández 2006). Nematodes and hymenopteran endoparasitoids can also transmit IIVs by introducing virus particles into susceptible hosts during the act of host penetration or oviposition, respectively (Mullens et al. 1999, López et al. 2000). Vertical transmission from parent to offspring has been demonstrated in the mosquito Ochlerotatus taeniorhynchus (Wiedemann) (Linley & Nielsen 1968a,b; Hall & Anthony 1971).

To accommodate the growing number of hosts reported with IIV infections, an interim system of nomenclature was proposed in which these viruses were assigned type numbers based on the chronological order in which they were reported (Tinsley & Kelly 1970). As such, Invertebrate iridescent virus 6 (IIV-6) is the type species of the Iridovirus genus that currently comprises two species (IIV-1 and IIV-6), and eleven tentative species of interrelated viruses with a dehydrated particle diameter in the range 110-160 nm. In contrast, the type species and sole member of the genus Chloriridovirus is Invertebrate iridescent virus 3 (IIV-3), which is the most studied member of the large IIVs that have a dehydrated particle diameter in the range 170-200 nm (Chinchar et al. 2005).

In an effort to stimulate research on this intriguing, yet poorly understood group of viruses, I have generated this annotated list of reported natural host species. The list does not include laboratory host range studies that are aimed at determining taxonomic limits to virus replication and which are not usually representative of the transmission opportunities available to IIVs infecting natural host populations. Examination of the list reveals the diversity of invertebrate hosts of iridoviruses and highlights some important areas for future study.

Compilation and Analysis of the Host List

The present host list was compiled from that given in Hall (1985) and updated by searching the following online databases: Web of Science (Thompson ISI), CABI SilverPlatter abstracts, ScienceDirect (www.info.sciencedirect.com), PubMed (www.ncbi.nlm.nih.gov/entrez) and Google Scholar (scholar.google.com). The principal search terms employed were iridovirus, iridescent virus and Iridoviridae. Selected sources included those that appeared in national and international scientific journals, the great majority of which were peer-reviewed, and book chapters published by well-established editorial houses (Elsevier, CRC, Plenum, etc.). Moreover, the references cited in each report were carefully examined for evidence of additional records of invertebrate hosts.

As many of the records of IIV infections date from before the modern era of molecular virology, the criteria used for assuming a putative IIV infection were mainly based on pathology and particle morphology. Among the principal criteria for inclusion in the annotated list were (i) characteristic iridescent signs of infection observed in host tissues, particularly in the epidermis and fat body, (ii) electron microscopy (EM) observation of icosahedral particles with an electron dense core and an internal lipid membrane of the correct size range (110-200 nm diameter) located in the cell cytoplasm, (iii) evidence of DNA genome, (iv) EM studies on particle ultrastructure, stages of replication and cellular pathology, (v) serological cross-reactivity with IIV antisera, (vi) molecular genetic and sequence information (for the most recently described isolates).

For each record the following information was registered: host species, country in which the infected invertebrate was found (including State in the case of the United States), prevalence of infected individuals, particle dimensions in ultrathin section or by negative staining, the original reference and any additional information on signs and characteristics of disease, circumstances surrounding the collection (such as habitat), other infected species present at the moment of collection, taxonomic status of the virus (when appropriate), and additional references containing characterization information for the isolate in question. As there are several examples of IIVs that can naturally infect different host species, reports of infections from the same host species in different countries were listed in chronological order. In most cases, no information exists to indicate whether such records relate to strains of the same virus species or not.

Invertebrate Host Diversity of Iridoviruses

A total of 79 scientific articles were identified with original information on the occurrence of confirmed and putative IIV infections in a total of 108 invertebrate species (Table 1). The great majority of these were arthropods (N = 103; 95%), and the remainder were molluscs, an annelid worm and a nematode. The list included nine species from marine habitats. Of the 99 species that were not marine, 49 were from terrestrial habitats and 50 were aquatic, comprising mainly the aquatic immature stages of Diptera (44 species), nymphs of Ephemeroptera (two species), daphnids (two species) and a freshwater snail (one species).

It is intriguing to note that many records from nematocerous Diptera relate to species of Aedes,Ochlerotatus (many of which were previously classified as Aedes) and Psorophora, but there are no records for Anopheles or Uranotaenia and only a single record for Culex and Culiseta. It is likely that these occurrences reflects some aspects of the biology or ecology of these mosquitoes because species of Anopheles,Culex and Culiseta can be infected with IIV-6 in the laboratory (Fukuda 1971), but not with IIV-3, which naturally only infects the saltmarsh mosquito, O. taeniorhynchus (Woodard & Chapman 1968).

This may be related to the survival of IIV particles in mosquito eggs (vertical transmission) as species of Aedes,Ochlerotatus and Psorophora have diapausing eggs, whereas the other genera normally do not. Alternatively, this may be due to behavioural differences as the cannibalistic habits of certain genera are an effective means of IIV transmission (Woodard & Chapman 1968, Marina et al. 2005). Different genera also have distinct thermal requirements during immature development and the replication of IIVs is thermolabile with complete inhibition at temperatures over 30°C. Finally, the turbidity of the aquatic habitat may affect the titres of suspended IIV particles which are readily adsorbed by clay particles (Christian et al. 2006), leading to sedimentation of virus particles and a reduced probability of transmission in the turbid waters inhabited by certain mosquitoes.

Another notable aspect of the host range of IIVs is that the majority of early isolates were from insects and, as such, IIVs attracted the attention of insect pathologists and were considered to be entomopathogens (Kelly 1985). However, the revision of the present list reveals that one third of the known host species are not insects. Records from terrestrial isopods (woodlice, sowbugs, pillbugs, etc.) are numerous, although the diversity of IIVs that infect them is mostly unstudied. There are also an appreciable number of records from molluscs and decapods. Comparisons of these isolates, several of which are from marine habitats, with those from insects have only been performed in two cases. In a recent record from a Nautilus sp. (Mollusca), PCR amplified DNA sequences indicated the iridovirus from this organism was more similar to those of ranaviruses than to insect iridoviruses (Gregory et al. 2006). This contrasts with a partial major capsid protein sequence recently reported from a sergestid shrimp, Acetes erythraeus, that showed ~80% similarity to sequences from insect iridoviruses (Tang et al. 2007). A single report of IIV particles causing disease in reptiles (Just et al. 2001) is unprecedented and requires validation (Williams et al. 2005).

Examination of the cumulative number of scientific reports of novel hosts to IIV infections (excluding reports of marine species) over time (Fig. 1A) reveals a slightly sigmoidal tendency with a slow rate of publication in the 10-15-year period following the first report of IIV infection by Xeros (1958), followed by an increased rate of publication from 1968 to 1990 and then a slowing rate of publication from 1990 to the present. Correspondingly, the cumulative number of host species reported with confirmed or putative IIV infections over time (Fig. 1B) followed a similar trend, but with a more stepped pattern with a number of new species being reported in the late 1970's and early 1980's followed by a low rate of new reports until 1999 when several more species were reported. The current rates of publication and new species records doubtless reflect a reduction in the number of active insect pathologists in recent years and a low interest in these pathogens for biological control purposes.

Geographical Distribution of Invertebrate Iridoviruses

Species with IIV infections have been reported from every continent, except Antarctica, but there is a noticeable abundance of records from northern Europe and the United States and a paucity of records from Africa, southern Asia and Latin America (with the exception of two studies on blackflies in Mexico and Guatemala). Evidently, this reflects the distribution of insect pathologists rather than the true distribution of hosts to IIVs. The need for greater study on IIVs from these parts of the world is underlined by the case of the mopane worm, Imbrasia belina (Westwood), which is eaten for food in several countries of southern Africa and which is periodically affected by epizootics of IIV disease leading to severe economic losses (Knell 2006). Similarly, very little is known about IIV infections of the Indian honeybee, Apis cerana Fabr., that can severely affect bee colonies in southern Asia and that may interact with the parasitic mite Varroa destructor Anderson & Trueman, (Camazine & Liu 1998).

Prevalence of Iridovirus Infections

It is evident from the host list that in most cases, IIV infections of insects and other invertebrates are rare, with just single or small numbers of patently infected specimens present in samples of hundreds or thousands of seemingly healthy individuals. However, in the case of natural populations of blackflies and mayflies and laboratory populations of Aedes aegypti (L.), the prevalence of covert infection is between 10 and many thousands of times that of patent infections (Williams 1993, 1995; Marina 1999, 2003; Tonka & Weiser 2000). In contrast, covert infections are rarely observed in terrestrial isopods or Spodoptera frugiperda (J. E. Smith). Clearly, IIV infection strategies and the factors that determine their virulence require considerable research. It is noticeable however, that abundant patent infections have been observed in high density populations of crickets, blackflies and some moths.

On occasions, iridovirus diseases have severely affected oyster populations in France and North America (Anthony & Comps 1991). However, for most other marine species, putative iridovirus infections have been detected serendipitously while studying some other aspect of host biology, and most hosts showed no signs of disease.

Relationship between Particle Size and Iridescence

The genome of the chloriridovirus IIV-3 differs significantly from those of members of the Iridovirus genus (Delhon et al. 2006). However, it is uncertain whether IIVs with large diameter particles represent a distinct genetic group due to the absence of genome sequence information from large IIVs. Nonetheless, particle size is the most obvious characteristic that currently defines the two invertebrate genera. Large particles have large interparticle distances and it is the distance between planes of particles in paracrystalline arrays that creates the iridescent hues seen in patently infected hosts. As such, colour is an immediate visual indicator of approximate particle size. Violet, blue and turquoise colours are usually generated by small particles in the range 110-130 nm diameter (when dehydrated and measured in ultrathin section), whereas green, yellow and orange hues are likely to be seen when cells are infected with large particles (160-200 nm diameter). Light reflected from the surface of paracrystalline arrays of virus particles interferes with incident light resulting in Bragg diffraction, thus causing the iridescent hues of heavily infected hosts.

The list includes some exceptions to this principle, for example a yellow-brown infection of Ochlerotatus sollicitans (Walker) was reported to involve particles with a diameter of 110 nm (Becnel & Fukuda 1989) and violet and blue infections of Culiseta annulata (Schrank) (Buchatsky 1977) and Aedes cantans (Meigen) (Buchatsky & Sherban 1976) were reported to involve particles with diameters of 180 and 200 nm, respectively. This can only be explained if paracrystalline arrays are unusually closely packed in the case of Cu. annulata and Ae. cantans or unusually separated in the case of O.sollicitans, or if measurements had been performed on material that had been unduly affected by laboratory processing. Indeed, the validity of using particle measurements as a key characteristic for classification has been questioned due to the variability in preparation and processing procedures between laboratories (Hall 1985).

The presence of an external fringe of fibrils that extend from the surface of the capsid can increase interparticle distance and thereby modulate the iridescence of infected hosts (Stoltz et al. 1968, Yan et al. 2000). The optical properties of IIVs have been explored using monochromatic light (Klug et al. 1959) and more recently using X-ray and thin film techniques (Juhl et al. 2004, 2006). It is notable that icosahedral particles from oysters have very large diameter particles (up to 380 nm), but the genetic characteristics of these marine viruses and their relationship to IIVs from terrestrial insects are unknown.

Identity of Putative Iridovirus Infections

It is evident that the majority of IIVs lack any characterization information. Indeed, despite the abundance of records in mosquitoes and midges of medical or veterinary importance it is noticeable that virtually no characterization data exist for these isolates, with the exception of IIV-3, the genome of which has recently been entirely sequenced (Denholm et al. 2006). Moreover, of the 74 records of IIVs in insect species, only 24 have partial characterization data and only two have been subjected to complete genome sequencing (Jakob et al. 2001, Denholm et al. 2006). It is known that certain IIVs, such as IIV-9 or IIV-31, naturally infect various host species (Cole & Morris 1980, Williams & Cory 1994), whereas others, such as IIV-3, are believed to be restricted to single species in nature. The true natural host range of these viruses will only be determined by extensive characterization studies from a range of different host species from different habitats. This also applies to the uncharacterized viruses from marine invertebrates.

Conclusions

Examination of the host list presented here gives rise to a number of conclusions:

(i) Of the 108 species reported as natural invertebrate hosts to confirmed and putative iridovirus infections the majority (69%) are insects or terrestrial isopods (18%), and nine species are from marine habitats.

(ii) The most common hosts are the aquatic stages of Diptera, particularly mosquitoes, yet these infections remain extremely poorly studied. The reasons that no infections have been reported from species of Anopheles and only a single report from Culex remain unknown.

(iii) The publication rate of new host species underline the current lack of interest generated in this group of viruses despite important advances in our understanding of their survival strategies, particularly the importance of covert infections that have significant effects on a number of fitness correlates in adult insects.

(iv) Additional studies are required, specifically to elucidate the identity and host range of IIVs infecting mosquitoes and to clarify the relationship of the iridoviruses from marine hosts to the other members of this family. In particular, a greater quantity and a greater diversity of genome sequence information is needed in order to define both intra- and inter-species variation in this intriguing, yet neglected, group of invertebrate viruses.

Acknowledgments

My thanks to Misha Yu. Sokolov (ECOSUR, Mexico) for careful reading of texts in Russian and Carlos F. Marina (CRISP-INSP, Mexico) for discussion of mosquito biology.

Received 30/VIII/06. Accepted 24/X/08.

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Publication Dates

• Publication in this collection
  16 Jan 2009
• Date of issue
  Dec 2008

History

• Received
  30 Aug 2006
• Accepted
  24 Oct 2008