Nosema ceranae, a newly identified pathogen of Apis mellifera in the USA and Asia Yan Ping Chen, Zachary Y. Huang To cite this version: Yan Ping Chen, Zachary Y. Huang. Nosema ceranae, a newly identified pathogen of Apis mellifera in the USA and Asia. Apidologie, Springer Verlag, 2010, 41 (3), 10.1051/apido/2010021. hal-00892100 HAL Id: hal-00892100 https://hal.archives-ouvertes.fr/hal-00892100 Submitted on 1 Jan 2010 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Apidologie 41 (2010) 364–374 Available online at: c INRA/DIB-AGIB/EDP Sciences, 2010 www.apidologie.org DOI: 10.1051/apido/2010021 Review article Nosema ceranae, a newly identified pathogen of Apis mellifera in the USA and Asia* YanPingChen1, Zachary Y. Huang2 1 USDA-ARS, Bee Research Laboratory, Beltsville, 20705 Maryland, USA 2 Department of Entomology, Ecology, Evolutionary Biology and Behavior, Michigan State University, East Lansing, MI 48824, USA Received 9 November 2009 – Revised 12 February 2010 – Accepted 24 February 2010 Abstract – Globalization has provided opportunities for parasites/pathogens to cross geographic boundaries and expand to new hosts. Nosema disease is one of the most serious adult honey bee diseases and has high prevalence in honey bee colonies. For years, Nosema apis was thought to be the only microsporidian infecting domestic bee colonies. However, recently it was discovered that N. ceranae could cross the species barrier from Asian honey bees (Apis cerana) to European honey bees (Apis mellifera) that are widely used for crop pollination and honey production. Over the last few years, considerable progress has been made in our understanding of Nosema infections in honey bees. This review summarizes previous findings and recent progress in the understanding of Nosema infection of A. mellifera in the USA and Asia, with particular emphasis on the comparative epidemiological, morphological, pathological, and genomic organization of two Nosema species. The prospects of future research and remaining unresolved questions associated with the study of honey bee Nosema diseases are also discussed. Nosema apis / N. ceranae / host range / distribution / morphology / pathology / genome 1. INTRODUCTION to A. mellifera was reported in Europe (Higes et al., 2006;Paxtonetal.,2007), United States Nosemosis (Nosema disease) is one of the (Chen et al., 2007), China (Liu et al., 2008), most serious and prevalent adult honey bee Vietnam and worldwide (Klee et al., 2007). diseases worldwide (Bailey, 1981; Matheson, Since its emergence as a potentially virulent 1993;Fries,2010) and is caused by intracel- pathogen of A. mellifera, N. ceranae has been lular microsporidian parasites from genus of associated with colony collapse of honey bees Nosema. For decades, Nosema disease was (Higes, et al., 2008; Paxton, 2010). A recent exclusively attributed to a single species of study showed that N. ceranae expanded its Nosema, N. apis, which was first described in host range to South American native bumble- European honey bees, Apis mellifera (Zander, bees (Plischuk et al., 2009) causing a new epi- 1909). In 1996, a new species of Nosema was demiological concern for this pathogen. The first discovered in the Asian honey bee, Apis present review summarizes recent findings on cerana, thus named Nosema ceranae (Fries Nosema ceranae infection of A. mellifera in et al., 1996). In 2005, a natural infection the USA and Asia, with particular emphasis on of N. ceranae was reported in A. mellifera the comparative epidemiological, morphologi- colonies from Taiwan (Huang et al., 2005). cal, pathological, and genomic analysis of two Shortly thereafter, the infection of N. ceranae Nosema species. Corresponding author: Y.P. Chen, [email protected] * Manuscript editor: Yves Le Conte Article published by EDP Sciences Nosema ceranae, a new pathogen of Apis mellifera 365 2. THE PREVALENCE OF NOSEMA that the infection rate of N. ceranae was sig- INFECTION IN THE UNITED nificantly higher than that of N. apis in bees STATES from both CCD affected colonies and normal healthy colonies (Cox-Foster et al., 2007). A A study for screening the prevalence of similar result was obtained from a more re- Nosema infections in the USA population of cently conducted CCD descriptive epidemio- A. mellifera was conducted in 2007 (Chen logical study (vanEngelsdorp et al., 2009). The et al., 2007). Bee samples collected between studies showed that the infection rate of N. cer- 1995 and 2007 from different geographic re- anae was 55% and 50% in CCD and control gions of the USA were examined individu- colonies, respectively, while the infection rate ally for the presence of both N. apis and of N. apis was 29% and 18% in CCD and con- N. ceranae using the PCR method. The re- trol colonies, respectively. All of these results sults showed that N. ceranae had a wide- were in line with a previous report that prior to spread infection of A. mellifera in the USA. 2003 most bee samples had N. apis infection N. ceranae infected bees were found in sam- but N. ceranae became a predominant infec- ples collected from each of 12 states includ- tion after 2003 (Klee et al., 2007). The stud- ing Oregon, California, Hawaii, Idaho, North ies conducted in the USA confirm and extend Dakota, Minnesota, Texas, Ohio, Tennessee, early observations by Fries et al. (2006), Higes Connecticut, Maryland and Florida, represent- et al. (2006, 2007)andHuangetal.(2007) ing the Northeast, Southeast, Midwest, South- that N. ceranae was not restricted to its origi- west, and the West regions of the USA Among nal host, but has established an infection in the the 180 bees examined for Nosema, 16% of European honey bee for some time, and that the bees were positive for N. ceranae, while infection with N. ceranae is now more com- N. apis was not detected. The absence of N. monthaninfectionwithN. apis in European apis may have been caused by inadequate sam- honey bees. pling. The detection of N. ceranae in honey bees collected in 1995 indicated that N. cer- anae is not a new emerging pathogen for A. 3. THE PREVALENCE OF NOSEMA mellifera in the USA and, in fact, had trans- INFECTION IN EAST ASIA ferred from its presumed original host A. cer- AND AUSTRALIA ana at least a decade ago. Although the data presented in this study demonstrated that N. A survey for the infection of A. mellifera ceranae infection was widespread in the USA, with both N. ceranae and N. apis was per- the authors believed that distribution of N. cer- formed in China (Liu et al., 2008). The sam- anae infection of A. mellifera could be even ples of honey bees were collected from 12 dif- more widespread than had been identified, if ferent apiaries located in ten provinces and two a more intensive epidemiological investiga- municipalities in China. Thirty bees from each tion was conducted. Later work by Williams apiary were pooled together and examined for et al. (2008) detected infection of N. ceranae the presence of N. ceranae and N. apis using in honey bees from the Maritime Provinces thePCRassay(Liuetal.,2008). N. ceranae of Canada and Minnesota, USA and expanded were found to be present in every apiary exam- the known distribution of this parasite. ined. Sequence comparison of PCR fragments While Chen et al. (2007) reported that PCR generated from the study with published se- amplification using N. apis specific primers quences at the GenBank resulted in 99% se- did not yield any positive results for bee quence identity for N. ceranae and confirmed samples tested, a study by the consortium the specificity of the PCR assay. No N. apis scientists using a metagnomic approach to was detected in any samples examined. survey microflora in Colony Collapse Disor- In contrast to the finding in the USA and der (CCD) affected bee colonies and healthy China that N. ceranae was identified as the colonies showed that co-infections of N. apis sole or predominant infection in A. mellifera, and N. ceranae were found in A. mellifera,and bee samples from Australia showed a notably 366 Y.P. Chen, Z.Y. Huang higher rate of N. apis infection (46.3%) than was 100 times higher than the copy number of N. ceranae infection (15.3%) (by calculation N. apis in coinfected bees (Chen et al., 2009b). from Table 2, Giersch et al., 2009). While The study indicates that host shifting also oc- N. ceranae was detected in samples collected curred for N. apis, in that N. apis not only from only four states (Queensland, New South attacks European honey bees but also Asian Wales, Victoria, and South Australia), N. apis honey bees and that N. ceranae is also the was found in samples collected from every more common and predominant infection of state. Among the 307 bees examined for infec- the two Nosema species in Asian honey bees. tion, only two bees had co-infection of both Nosema species. Further, the prevalence of N. ceranae infection varied considerably across 4. COMPARATIVE states. While Western Australia and Tasma- MORPHOLOGICAL, nia were found to have no incidence of N. PATHOLOGICAL, AND GENOMIC ceranae infection, N. ceranae was detected in ANALYSIS OF NOSEMA 33.7%, 16%, 15.8%, and 4.5% of bees col- lected in Queensland, South Australia, New 4.1. Morphology South Wales, and Victoria, respectively.