Australian bat coronaviruses

Abstract

Coronaviruses were responsible for the global outbreak of severe acute respiratory syndrome (SARS) in 2003 and 2004, and the outbreak of Middle East respiratory syndrome (MERS) in 2012. Bats have since been identified as the natural hosts for a number of novel coronaviruses, including the likely ancestors to SARS and MERS coronaviruses. It is essential for Australia’s biosecurity preparedness, and for broader understanding of this previously unknown group of viruses, that coronaviruses in bats in our region are identified, characterised and their ecology understood.

In Chapter 1, the relevant literature is reviewed, both in the context of my contribution to the Food and Agricultural Organisation of the United Nations publication ‘Investigating the Role of Bats in Emerging Zoonoses’, and additionally in updating subsequent research and emergence events.

Chapter 2 presents a novel peer reviewed and published methodology for collecting blood samples from small bats. This methodology was essential for the studies that followed.

Chapter 3 reports on the surveillance of 2,195 bats from Australia and neighbouring countries sampled between 1997 and 2009 for evidence of coronavirus infection. The study identified coronaviruses belonging to two genera (Alpha- and Betacoronavirus) in Australian bats, and serological evidence of infection of coronaviruses in bats from East Timor, Indonesia, Malaysia and Papua New Guinea. It also identified an interspecies transmission of a variant of the alphacoronavirus Miniopterus bat coronavirus HKU8 from Miniopterus spp bats to bats of the genus Rhinolophus, supporting the hypothesis that bats from this genus are more likely to foster host shifts and pose a risk for the emergence of other bat coronaviruses. The study also elucidated the current diversity of coronaviruses in Queensland bats, and the findings are consistent with co-evolution with the occasional fostering of host shifts by bats of the genera Hipposideridae and Rhinolophidae. Further, they suggest that bat coronaviruses are as old as the most common bat ancestor - 65 million years.

Chapter 4 presents a longitudinal study of bats inhabiting an abandoned gold mine, which were sampled during spring, summer, autumn and winter between 2006 and 2008. The data and models from this study were used to develop a hypothesis of the infection dynamics of a novel Alphacoronavirus in Miniopterus spp. The hypothesis utilises a classical susceptible-infected-recovering (SIR) model, with individuals either susceptible to Australian bat coronaviruses 3 infection, infected, or recovering from infection. An extension of the model considers pups that receive maternal antibody protection and tracks their progression through states of disease using a MSIR model, where a state of maternally derived immunity exists prior to becoming susceptible to infection. The findings suggested that bats have an anamnestic (immunological) memory which limits secondary coronavirus infections with a stronger and more rapid production of antibodies, compared to a primary infection.

In Chapter 5, a modified mark/recapture study on a maternal population of the Australian bat Myotis macropus identified that individual bats were infected with a novel unclassified putative Alphacoronavirus for up to 11 weeks. The observed pattern of infection supports not only a hypothesis of persistent coronavirus infection in bats, but also suggests that acute infection, and intermittent viral is possible.

The work in this thesis has made a major contribution to understanding the diversity and ecology of coronaviruses in bats. The findings have implications not only for Australia, where most of the studies were based, but also for the international community. The research highlighted the broad distribution of bat coronaviruses, both geographically and across bat species, demonstrated the risk of interspecies transmission, and modelled the infection dynamics of the viruses within individual bat species.