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Dynamic Subspecies Population Structure of Vibrio cholerae in Dhaka, Bangladesh

Abstract

Cholera has been endemic to the Ganges Delta for centuries. Although the causative agent, Vibrio cholerae, is autochthonous to coastal and brackish water, cholera occurs continually in Dhaka, the inland capital city of Bangladesh which is surrounded by fresh water. Despite the persistence of this problem, little is known about the environmental abundance and distribution of lineages of V. cholerae, the most important being the pandemic generating (PG) lineage consisting mostly of serogroup O1 strains. To understand spatial and temporal dynamics of PG lineage and other lineages belonging to the V. cholerae species in surface water in and around Dhaka City, we used qPCR and high-throughput amplicon sequencing. Seven different freshwater sites across Dhaka were investigated for six consecutive months, and physiochemical parameters were measured in situ. Total abundance of V. cholerae was found to be relatively stable throughout the 6-month sampling period, with 2 × 105 to 4 × 105 genome copies/L at six sites and around 5 × 105 genome copies/L at the site located in the most densely populated part of Dhaka City. PG O1 V. cholerae was present in high abundance during the entire sampling period and composed between 24 and 92% of the total V. cholerae population, only showing occasional but sudden reductions in abundance. In instances where PG O1 lost its dominance, other lineages underwent a rapid expansion while the size of the total V. cholerae population remained almost unchanged. Intraspecies richness of V. cholerae was positively correlated with salinity, conductivity, and total dissolved solids (TDS), while it was negatively correlated with dissolved oxygen (DO) concentration in water. Interestingly, negative correlation was observed specifically between PG O1 and salinity, even though the changes in this variable were minor (0–0.8 ppt). Observations in this study suggest that at the subspecies level, population composition of naturally occurring V. cholerae can be influenced by fluctuations in environmental factors, which can lead to altered competition dynamics among the lineages.

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Fig. 1

adapted from Khatun et al. [54]

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Data Availability

All the genome sequences and relevant genomic and epidemiological data related to the isolates used are publicly available on PubMLST (https://pubmlst.org/vcholerae/).

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Acknowledgements

MA of icddr,b thanks the government of Bangladesh, Canada, Sweden, and UK for providing unrestricted core support.

Funding

This work was supported by the Natural Sciences and Engineering Research Council of Canada (NSERC) and the Integrated Microbial Biodiversity program of the Canadian Institute for Advanced Research to YB. We also acknowledge the support of graduate student scholarships from NSERC to TN, and Alberta Innovates Technology-Futures and Faculty of Graduate Studies and Research to TN, MTI, and KYHL.

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Authors

Contributions

YB, TN, MTI, and MA designed the project. TN, MTI, and YB wrote the manuscript. MTI, FTJ, MS, and MA helped perform the sample collection and sample processing during field trips in Dhaka, Bangladesh. TN performed the qPCR, and MTI did the amplicon sequencing. TN and MTI did the data analysis. KYHL helped in the bioinformatics analysis. MTI, YB, FTJ, MS, RJC, and MA reviewed the manuscript. MA and YB supervised the project.

Corresponding author

Correspondence to Yann F. Boucher.

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The authors declare no competing interests.

Additional information

Importance

Although Vibrio cholerae has been studied for decades as a human pathogen, little is known about its abundance and population structure in the environment before an outbreak. In this study, we have employed high-throughput amplicon sequencing of a species-specific region within a protein-coding gene (viuB) to track subspecies lineages of V. cholerae, including the PG lineage responsible for cholera, in an urban region endemic for cholera. Coupled with real-time qPCR, this method provided subspecies-level resolution of the abundance and lineage composition of V. cholerae populations. This is a key to understanding how intraspecies diversity could play a role in regulating the abundance of pandemic V. cholerae, with environmental factors contributing to the relative fitness of different lineages.

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Nasreen, T., Islam, M.T., Liang, K.Y.H. et al. Dynamic Subspecies Population Structure of Vibrio cholerae in Dhaka, Bangladesh. Microb Ecol (2021). https://doi.org/10.1007/s00248-021-01838-0

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Keywords

  • Vibrio
  • V. cholerae
  • Cholera
  • Endemic
  • Pandemic
  • Pandemic generating lineage
  • Subspecies
  • Populations
  • Tania Nasreen and Mohammad Tarequl Islam authors contributed equally