Novel Alphacoronaviruses and Paramyxoviruses Cocirculate with Type 1 and Severe Acute Respiratory System (SARS)-Related Betacoronaviruses in Synanthropic Bats of Luxembourg

Abstract

Several infectious disease outbreaks with high mortality in humans have been attributed to viruses that are thought to have evolved from bat viruses. In this study from Luxembourg, the genetic diversity and epidemiology of paramyxoviruses and coronaviruses shed by the bat species Rhinolophus ferrumequinum and Myotis emarginatus were evaluated. Feces collection (n ϭ 624) was performed longitudinally in a mixed-species colony in 2015 and 2016. In addition, feces (n ϭ 254) were collected cross-sectionally from six Myotis emarginatus colonies in 2016. By use of degenerate primers in a nested format, overall prevalences of 1.1% (10/878) and 4.9% (43/878) were determined for paramyxoviruses and coronaviruses. Sequences of the partial RNAdependent RNA polymerase and spike glycoprotein genes of coronaviruses, as well as sequences of the partial L gene of paramyxoviruses, were obtained. Novel paramyxovirus and Alphacoronavirus strains were identified in different Myotis emarginatus colonies, and severe acute respiratory syndrome (SARS)-related Betacoronavirus strains were shed by Rhinolophus ferrumequinum. Logistic regression revealed that the level of Alphacoronavirus shedding was highest in July (odds ratio, 2.8; P Ͻ 0.01), probably due to periparturient stress. Phylogenetic analyses point to close virus-host coevolution, and the high genetic similarity of the study strains suggests that the Myotis emarginatus colonies in Luxembourg are socially connected. Most interestingly, we show that bats also host Betacoronavirus 1 strains. The high similarity of the spike gene sequences of these viruses with mammalian Betacoronavirus 1 strains may be of concern. Both the SARS-related and Betacoronavirus 1 strains detected in bats in Luxembourg may cross the species barrier after a host adaptation process.IMPORTANCE Bats are a natural reservoir of a number of zoonotic pathogens. Several severe outbreaks in humans (e.g., a Nipah virus outbreak in Malaysia in 1998, and the almost global spread of severe acute respiratory syndrome in 2003) have been caused by bat-borne viruses that were transmitted to humans mostly after virus adaptation (e.g., in intermediate animal hosts). Despite the indigenousness of bat species that host viruses with suspected zoonotic potential and despite the zoonotic transmission of European bat 1 lyssavirus in Luxembourg, knowledge about the diversity and epidemiology of bat viruses remains limited in this country. Moreover, in contrast to other European countries, bat viruses are currently not included in the national surveillance activities of this land-locked country. We suggest that this gap in disease surveillance should be addressed, since we show here that synanthropic bats host viruses that may be able to cross the species barrier.

Geographical structure of bat SARS-related coronaviruses

“…In 2005, the discovery of novel CoVs related to human SARS-CoVs in Chinese horseshoe bats (genus Rhinolophus), named SARS-related coronaviruses (SARSr-CoVs), provided new clue that bats may be the natural host for SARS-CoV (Lau et al, 2005;Li et al, 2005). Since then, genetically diverse SARSr-CoVs have been discovered in Asia, Europe, and Africa, including China, South Korea, Thailand, Bulgaria, Slovenia, Italy, Luxembourg, Nigeria, and Kenya (Balboni et al, 2012b;Drexler et al, 2010;He et al, 2014;Lau et al, 2010;Lau et al, 2005;Li et al, 2005;Pauly et al, 2017;Ren et al, 2006;Rihtaric et al, 2010;Yang et al, 2013;Yuan et al, 2010). Importantly, it was reported that some bat SARSr-CoVs were able to use angiotensin converting enzyme II (ACE2) from humans, civets and Chinese horseshoe bats as a receptor originated from Chinese horseshoe bats and suggesting that these SARSr-CoVs had the ability to infect humans immediately without other intermediate hosts.…”

Circulation of Alphacoronavirus, Betacoronavirus and Paramyxovirus in Hipposideros bat species in Zimbabwe

“…However, the Beilong virus was discovered on human kidney cell lines and neutralising antibodies against J virus have been detected in rodents, pigs and humans (Audsley et al, 2016). In addition, bat viruses belonging to the related-Jeilongvirus genus were widely detected in China and more recently in Luxembourg in Europe (Pauly et al, 2017). Altogether, these data highlight the need for further studies on the zoonotic potential of these viruses.…”

Coronavirus and paramyxovirus in bats from Northwest Italy

“…Several alpha and beta-CoVs have been described worldwide in different bat species (e.g. [9][10][11][12][13][14][15][16][17]). From the first report in China, Rhinolophus species have been specifically associated with SARS-like CoVs [18][19][20], belonging to the lineage b of beta-CoV genus.…”

“…Moreover, the ever-increasing attention paid to bat-associated pathogens, has led to the discovery of numerous novel and yet unclassified PMV, revealing an unexpected genetic diversity in the Paramyxovirinae subfamily [36]. PMV identification has been reported in only few studies in insectivorous bats in Europe from Germany, Bulgaria, Romania and Luxembourg, with none of the novel viruses closely related with highly or human pathogenic paramyxoviruses [16,17,27,36].…”