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Enemies With Benefits

Viruses represent some of the deadliest pathogens known to science. Recently they have been reported to have mutualistic interactions with their hosts, providing them direct or indirect benefits. The mutualism and symbiogenesis of such viruses with lower eukaryotic partners such as fungi, yeast, and insects have been reported but the full mechanism of interaction often remains an enigma. In many instances, these viral interactions provide resistance against several biotic and abiotic stresses, which could be the prime reason for the ecological success and positive selection of the hosts. These viruses modulate host metabolism and behavior, so both can obtain maximum benefits from the environment. They bring about micro- and macro-level changes in the hosts, benefiting their adaptation, reproduction, development, and survival. These virus-host interactions can be bilateral or tripartite with a variety of interacting partners. Exploration of these interactions can shed light on one of the well-coordinated biological phenomena of co-evolution and can be highly utilized for various applications in agriculture, fermentation and the pharmaceutical industries.

Enemies with Benefits


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Positive and negative aspects of species interactions can be context dependant and strongly affected by environmental conditions. We tested the hypothesis that, during periods of intense heat stress, parasitic phototrophic endoliths that fatally degrade mollusc shells can benefit their mussel hosts. Endolithic infestation significantly reduced body temperatures of sun-exposed mussels and, during unusually extreme heat stress, parasitised individuals suffered lower mortality rates than non-parasitised hosts. This beneficial effect was related to the white discolouration caused by the excavation activity of endoliths. Under climate warming, species relationships may be drastically realigned and conditional benefits of phototrophic endolithic parasites may become more important than the costs of infestation.

Endoliths are metabolically dependent to their host; excavation into the host shell is through chemical dissolution, with the carbonate ions released being converted from calcite into CO2 that is then used for photosynthesis10. Because of their boring activity, these parasites cause a distinctive discoloration of the outer layer of the mussel shell11. In this study, we consider a situation in which shell-degrading endoliths could benefit their hosts. Specifically, we hypothesise that parasites lower host body temperatures during low tide aerial exposure by either enhancing solar reflectivity as a result of the whitening of the shell or by dissipating heat through photosynthetic activity. If so, we predicted that, during periods of intense heat stress, non-infested mussels would suffer higher mortality rates than those that are infested.

Climate change will not involve an increase in heating through solar radiation, but during aerial exposure mussels lose heat to the surrounding air by convection, radiation and conduction. Critically, rates of heat loss through conduction are proportional to the temperature gradient between the mussel and its surroundings, which will decrease as air temperatures rise. In this situation, the effect of minimising solar heating through shell discolouration is likely to become increasingly advantageous. Gradual warming and increased frequency and duration of extreme heat-events14,15 will challenge both clean and infested individuals. As intertidal invertebrates are essentially marine species with many already living at or close to their upper thermal tolerance limits16, thermoregulatory discolouration caused by endolithic erosion may provide important ecological advantages. Indeed, temperature-driven mass mortalities of diverse intertidal organisms, including barnacles, limpets and mussels, have already been reported17,18.

To test whether endolithic photosynthetic activity caused reduced mussel body temperatures by intercepting light energy, IR images of biomimetic mussels made with shell valves with live or silenced (dead) endoliths were compared. Biomimetic mussels were built to mimic the thermal characteristics of living mussels adapted from36. They were filled with marine silicone sealant and left to dry at room temperature for 48h prior to the experiments. Endoliths were killed (hence photosynthetic activity silenced) by keeping the mussel shells in boiling water for an hour before assembly them.

How to cite this article: Zardi, G. I. et al. Enemies with benefits: parasitic endoliths protect mussels against heat stress. Sci. Rep. 6, 31413; doi: 10.1038/srep31413 (2016).

G.I.Z. and K.R.N. conceived the main ideas; G.I.Z., K.R.N., C.D.M., T.N., J.L. and L.S. contributed to research design, fieldwork, data analyses and interpretation; G.I.Z. and K.R.N. performed laboratory experiments; G.I.Z. and K.R.N. led the writing with substantial contributions from C.D.M., T.N., J.L. and L.S.

Three-way symbiotic relationship amongst plant, endophytic fungus and a virus. D. lanuginosum shows enhanced thermal tolerance [65 C]. This thermal tolerance is acquired due to the presence of a dsRNA virus CThTV residing within an endophytic fungus C. proturberta

It was reported that C. protuberata could colonize various plants such as Oryza sp., Triticum sp., Solanum lycopersicum and Cucurbita pepo [13]. In S. lycopersicum, thermal tolerance is observed when associated with CThTV infected C. proturberata [6, 14]. Thus, this mechanism of virus infection-mediated thermal protection can be applied to other plants for the development of abiotic stress tolerance.

Apart from wasps, mutualistic viruses are found in many other insects. A polyphagous lepidopteran Helicoverpa armigera is one of the most cosmopolitan crop pests. Chemical pesticides, genetically modified crops, and the use of viruses like baculoviruses as biopesticides are common practices for H. armigera control. Recently, H. armigera was found to show an increased resistance against major biopesticides due to the presence of H. armigera densovirus-2 (HaDV-2), previously known as H. armigera densovirus-1 (HaDNV1). HaDV-2 is a dsDNA virus classified within the family Parvoviridae, transmitted vertically through eggs. The genome of the virus is about 5 kb in size and contains 3 ORFs. ORF1 and 2 encode for non-structural (NS) proteins similar to helicase and NS2, respectively. ORF3 on the other hand, encodes a structural protein VP. Insects infected with the virus show an increase in lifespan, weight and fecundity as well as enhanced resistance to cry1Ac and H. armigera nucleopolyhedrovirus infection [Figure 4]. This suggests that HaDV-2 is a mutualistic virus, but its mechanism of interaction is still unknown [49]. Some plant viruses also show similar effects on their insect vectors. Feeding of thrip, Frankliniella occidentalis, on plants leads to the transmission of tomato spotted wilt virus. Larvae feeding on such virus-infected plants show rapid development, as compared to those feeding on non-infected plants [50]. Similarly, aphids Micromyzus kalimpongensis transmit cardamom bushy dwarf virus, which causes foorkey disease in large cardamom. This virus belongs to the genus Babuvirus of the virus family Nanoviridae. M. kalimpongensis carrying the virus show a significant increase in the fecundity, longevity and growth rate during nymphal instar [51].

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