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Origins of the Current Seventh Cholera Pandemic

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Origins of the Current Seventh Cholera Pandemic Origins of the current seventh cholera pandemic Dalong Hua,b,1,2,BinLiua,c,1,LuFenga,b,d, Peng Dinga,XiGuoa,MinWanga, Boyang Caoa,b,d, Peter R. Reevese,3, and Lei Wanga,b,d,f,3 aTEDA Institute of Biological Sciences and Biotechnology, Nankai University, Tianjin Economic-Technological Development Area, Tianjin 300457, People’s Republic of China; bThe Key Laboratory of Molecular Microbiology and Technology, Ministry of Education, Tianjin 300457, People’s Republic of China; cTianjin Research Center for Functional Genomics and Biochip, Tianjin 300457, People’s Republic of China; dTianjin Key Laboratory of Microbial Functional Genomics, Tianjin 300457, People’s Republic of China; eSchool of Life and Environmental Sciences, University of Sydney, Sydney, NSW 2006, Australia; and fState Key Laboratory of Medicinal Chemical Biology, Nankai University, Tianjin 300071, People’s Republic of China Edited by John J. Mekalanos, Harvard Medical School, Boston, MA, and approved October 11, 2016 (received for review June 2, 2016) Vibrio cholerae has caused seven cholera pandemics since 1817, im- V. cholerae strains are serogrouped based on their poly- posing terror on much of the world, but bacterial strains are cur- saccharide O antigens, and >200 serogroups have been identified rently only available for the sixth and seventh pandemics. The El Tor to date (6). However, most of the serogroup diversity is in biotype seventh pandemic began in 1961 in Indonesia, but did not nonpathogenic environmental strains, and all pandemic strains originate directly from the classical biotype sixth-pandemic strain. have been from a serogroup O1 clone or a serogroup O139 Previous studies focused mainly on the spread of the seventh pan- variant. Serogroup O1 strains are further classified into two demic after 1970. Here, we analyze in unprecedented detail the biotypes: “classical” (the biotype of the organisms first identified origin, evolution, and transition to pandemicity of the seventh-pan- as causing cholera) and “El Tor” (named after the El Tor demic strain. We used high-resolution comparative genomic analysis quarantine station in Egypt, where a strain of this biotype was of strains collected from 1930 to 1964, covering the evolution from first isolated in ∼1900). The two biotypes are usually distin- the first available El Tor biotype strain to the start of the seventh guished according to the presence of hemolysin and the presence pandemic. We define six stages leading to the pandemic strain and of the acetoin fermentation pathway, both of which are charac- reveal all key events. The seventh pandemic originated from a non- teristic of El Tor strains. Only strains from the sixth (1899–1923) pathogenic strain in the Middle East, first observed in 1897. It sub- and seventh (1961 to present) pandemics have been available for sequently underwent explosive diversification, including the modern scientific study. The sixth pandemic was caused by spawning of the pandemic lineage. This rapid diversification sug- classical biotype strains, whereas the ongoing seventh pandemic gests that, when first observed, the strain had only recently arrived was caused by El Tor biotype strains. Strains from the fifth in the Middle East, possibly from the Asian homeland of cholera. The pandemic were shown to be of the classical biotype, but no live lineage migrated to Makassar, Indonesia, where it gained the impor- strains remain. Additionally, a second pandemic genome se- tant virulence-associated elements Vibrio seventh pandemic island quence from a preserved human intestine grouped with sixth- I (VSP-I), VSP-II, and El Tor type cholera toxin prophage by 1954, and pandemic strains in a phylogenetic tree (7), indicating that all but it then became pandemic in 1961 after only 12 additional mutations. the seventh pandemic were caused by a single lineage of classical Our data indicate that specific niches in the Middle East and Makas- biotype. Although the currently available seventh- and sixth- sar were important in generating the pandemic strain by providing pandemic strains share a common ancestor, we have shown that gene sources and the driving forces for genetic events. the seventh-pandemic strain did not originate directly from the Vibrio cholerae | pandemic | evolution | comparative genomics Significance he bacterium Vibrio cholerae is the causative agent of cholera, Cholera, a major disease in human history, has terrorized the Ta severe and potentially life-threatening diarrheal disease world through seven pandemics. The seventh pandemic started that is of considerable public health concern because of its high in Indonesia in 1961 and spread globally, currently infecting 3–5 morbidity and mortality. There have been seven cholera pan- million people annually. By combining all available historical demics since 1817, and all continents except Antarctica have had records and genomic analysis of available preseventh pandemic significant or major incursions by one or more of them (1). As and some early pandemic strains, we revealed the complex six- early as 1866, an intergovernmental meeting on cholera was held step evolution of the pandemic strain from its probable origin in to develop measures for control, making V. cholerae one of the South Asia to its nonpathogenic form in the Middle East in ∼ ∼ first infectious pathogens subject to inspection and quarantine. 1900 to Indonesia in 1925, where it evolved into a pandemic The current seventh pandemic began in 1961 in Makassar, strain before becoming widespread in 1961. This pathway re- lates to human traffic routes, including the annual Hajj pilgrim- Sulawesi, Indonesia, and continues to be a major health problem, age, and involved novel niches that provided gene sources and with an estimated 3 million to 5 million cases of infection every the driving forces for stepwise evolution. year (2), including recent outbreaks in Haiti and Zimbabwe. The outbreak in Haiti after the 2010 earthquake infected nearly Author contributions: L.F., P.R.R., and L.W. designed research; D.H., B.L., P.D., X.G., M.W., 700,000 people and has caused >8,500 deaths (3). In the 2008 and B.C. performed research; D.H., B.L., L.F., P.R.R., and L.W. analyzed data; and B.L., P.R.R., Zimbabwe epidemic, >90,000 suspected cholera cases were and L.W. wrote the paper. reported, with >4,000 of these patients dying (4). Cholera is The authors declare no conflict of interest. characterized by an extreme form of watery diarrhea, which This article is a PNAS Direct Submission. causes dehydration that can be lethal. The major virulence fac- Data deposition: The sequences reported in this paper have been deposited in the Gen- – tors are the TcpA pilus for attachment of bacteria to the in- Bank database (accession nos. CP013301 CP013320). 1 testinal epithelium and the cholera toxin (CTX), which is D.H. and B.L. contributed equally to this work. 2 released and then enters epithelial cells, where it induces se- Present address: School of Life and Environmental Sciences, Charles Perkins Centre, D17, University of Sydney, Sydney, NSW 2006, Australia. cretion of the water and salts that are the major component of 3To whom correspondence may be addressed. Email: [email protected] or peter. the stools. The disease and virulence factors have been reviewed [email protected]. many times, and we suggest Harris et al. as suitable background This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. for this paper (5). 1073/pnas.1608732113/-/DCSupplemental. E7730–E7739 | PNAS | Published online November 14, 2016 www.pnas.org/cgi/doi/10.1073/pnas.1608732113 Downloaded by guest on September 30, 2021 sixth-pandemic strain (8). Note that we are using the word strain Makassar, as well as the currently available seventh-pandemic PNAS PLUS for two generally accepted meanings: (i) the progeny of a single strains, together provide an excellent opportunity for understanding cell, usually first isolated as a colony (examples being “strain how the seventh-pandemic strain originated. However, studies fo- N16961” and “seventh pandemic strains”) and (ii) a lineage that cused on these strains are currently rather limited. We previously occurs in nature (examples being “seventh pandemic strain” and used a complete genome sequence of one of them (M66-2) to “sixth pandemic strain”). The meaning can be deduced from identify some of the events that occurred on the pathway to the the context. seventh-pandemic strain (8). However, for the six other available Long before the seventh pandemic started in 1961, El Tor prepandemic strains, only three draft genome sequences (for A6, biotype strains from two small areas had been reported, com- MAK757, and NCTC8457) have been reported. In addition, studies monly referred to as Middle East and Makassar strains and on the seventh pandemic itself have focused on strains isolated after collectively as preseventh pandemic (or prepandemic) strains 1970 (22, 24), and there were no full genome sequences of seventh- (9). The Middle East strains, which were isolated from Mecca, pandemic strains isolated in the first 10 y of the pandemic. Thus, the Saudi Arabia, and adjacent areas extending into Egypt and Iraq, roles played by the Middle East and Makassar strains in the evo- were observed and studied from 1897 to 1938 (10–14) (see SI lution of the seventh-pandemic strain remain unknown, as well as Text for details and sources). These strains were found in human the many evolutionary events that occurred over the 60-y period intestines,
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