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Title: Emerging tuberculosis pathogen hijacks social communication behavior in the group-living banded mongoose (Mungos mungo)

item ALEXANDER, KATHLEEN - Virginia Tech
item SANDERSON, CLAIRE - Virginia Tech
item LARSEN, MICHELLE - Albert Einstein College Of Medicine
item ROBEE-AUSTERMAN, SUELEE - Animal And Plant Health Inspection Service (APHIS)
item WILLIAMS, MARK - University Of Pretoria
item Palmer, Mitchell

Submitted to: mBio
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 4/15/2016
Publication Date: 5/6/2016
Citation: Alexander, K.A., Sanderson, C.E., Larsen, M.H., Robee-Austerman, S., Williams, M.C., Palmer, M.V. 2016. Emerging tuberculosis pathogen hijacks social communication behavior in the group-living banded mongoose (Mungos mungo). mBio. 10:7(3). pii: e00281-16. doi: 10.1128/mBio.00281-16.

Interpretive Summary: In Northern Botswana, Africa a new species of bacteria, closely related to the bacteria that cause human and animal tuberculosis has been discovered. The organism is named Mycobacteria mungi (M. mungi) and is found in wild populations of banded mongoose. There is no evidence, so far, that M. mungi infects people or other animals. However, we have determined that the route of disease transmission occurring among mongoose is a novel one, not seen in other wild or domestic animals that develop tuberculosis. In humans, and many animals, tuberculosis is spread by aerosol transmission. In mongoose, M. mungi are found in the glands near the anus (anal glands). These glands contain an oily fluid used for marking territory. As mongoose discharge anal gland fluids to mark their territory they contaminate the environment with M. mungi. Other mongoose (often from completely different social groups) investigate the markings by sniffing and placing their own anal gland fluids over those of the previous animal. In the process bacteria enter the nasal cavity and get on the skin around the nose. In males, bacteria also get on the surface of the scrotum. One of the most common places to find tuberculosis in mongoose is the skin on the top of the nose and inside the nose. The infection spreads rapidly with infected mongoose developing tuberculosis in many organs. This novel transmission mechanism hijacks communication networks fundamental to group living thus transmitting disease to animals that otherwise would not have direct contact (i.e. different social groups).

Technical Abstract: Mycobacterium mungi, a novel M. tuberculosis complex pathogen (MtbC), has emerged in wild banded mongoose (Mungos mungo) in Northern Botswana, causing significant mortality. Unlike other members of the MtbC, M. mungi is not transmitted through a primary aerosol route. Rather, pathogen invasion occurs through lesions or breaks in the nasal planum and/or skin of the mongoose host. Lesions in the lung, when present, have only been identified in disseminated disease. To determine the source of environmental exposure, we collected samples from the home range of infected troops, evaluating human sewage (n=12), wildlife and domestic animal feces (n=121, 16 species), and soil (n=172) for M. mungi-specific DNA. We also sampled banded mongoose feces (n=113), urine (n=23), and anal gland tissue (n=18) and secretions (n=44) from infected troops. No environmental sources of M. mungi were found; however, 22% of urine samples, 33% of anal gland tissue, and 39% of anal gland secretions were infected with M. mungi. Data suggest M. mungi can be transmitted between mongooses through exposure to infected anal gland secretions and urine used in scent marking. These findings are consistent with macro- and microscopic observations that pathogen invasion occurs through injuries in the nose and/or skin, areas of the mongoose host in frequent contact with these secretions. As with other mammals, banded mongooses use anal gland secretions and urine to provide critical olfactory messages to conspecifics within and between social groups. This mode of disease transmission hijacks communication networks fundamental to group living, circumventing social barriers to pathogen spread.