Abstract
Wolbachia infections are a model for understanding intracellular, bacterial symbioses. While the symbiosis is often studied from a binary perspective of host and bacteria, it is increasingly apparent that additional trophic levels can influence the symbiosis. For example, Wolbachia in arthropods harbor a widespread temperate bacteriophage, termed WO, that forms virions and rampantly transfers between coinfections. Here we test the hypothesis that temperatures at the extreme edges of an insect's habitable range alter bacteriophage WO inducibility and in turn, Wolbachia densities and the penetrance of cytoplasmic incompatibility. We report four key findings using the model wasp, Nasonia vitripennis: First, both cold treatment at 18 C and heat treatment at 30 C reduce Wolbachia densities by as much as 74% relative to wasps reared at 25 C. Second, in all cases where Wolbachia densities decline due to temperature changes, phage WO densities increase and inversely associate with Wolbachia densities. Heat has a marked effect on phage WO, yielding phage densities that are 552% higher than the room temperature control. Third, there is a significant affect of insect family on phage WO and endoysmbiont densities. Fourth, at extreme temperatures, there was a temperature-mediated adjustment to the density threshold at which Wolbachia cause complete cytoplasmic incompatibility. Taken together, these results demonstrate that temperature simultaneously affects phage WO densities, endosymbiont densities, and the penetrance of cytoplasmic incompatibility. While temperature shock enhances bacteriophage inducibility and the ensuing bacterial mortality in a wide range of medically and industrially-important bacteria, this is the first investigation of the associations in an obligate intracellular bacteria. Implications to a SOS global sensing feedback mechanism in Wolbachia are discussed.
Highlights
The obligate intracellular bacteria, Wolbachia, live in a majority of arthropod species worldwide [1]
The penetrance of all of the major reproductive alterations caused by Wolbachia, including cytoplasmic incompatibility (CI), malekilling, parthenogenesis, and feminization, are correlated with bacterial densities, and such density effects are not confined to Wolbachia endosymbionts
To first characterize the effects of hot and cold temperatures on Wolbachia densities in N. vitripennis, we normalized absolute single gene copy counts from Real-time quantitative polymerase chain reaction (RT-qPCR) of the W. pipientis groEL gene to that of the N. vitripennis S6 kinase (S6K) gene
Summary
The obligate intracellular bacteria, Wolbachia, live in a majority of arthropod species worldwide [1]. While extensive work has been done to understand lysogeny and lytic induction in medically or industrially important bacteria, no studies have defined the parameters under which prophages are induced from obligate intracellular bacteria. While host and bacterial factors regulate Wolbachia densities in vivo, there are wellknown environmental variables (e.g., temperature, antibiotics, and host age) that can decrease Wolbachia densities and functions across many species [18,19,20,21]. Some of these same variables induce viron formation and the lytic lifecycle of temperate bacteriophage in free-living bacteria. While we are not testing the SOS mechanism per se, we aim to test if temperature triggers changes in the phage’s titer and whether this variation correlates with variation in the densities and penetrance of Wolbachia functions following environmental stress
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