Indian Journal of Microbiology

, Volume 59, Issue 2, pp 193–199 | Cite as

Prokaryotic Diversity in Oxygen Depleted Waters of the Bay of Bengal Inferred Using Culture-Dependent and -Independent Methods

  • Genevieve L. Fernandes
  • Belle D. Shenoy
  • Larissa D. Menezes
  • Ram M. Meena
  • Samir R. DamareEmail author
Original Research Article


There are regions in the world oceans where oxygen saturation is at its lowest, evident at depths between shelf to upper bathyal zone. These regions are known as Oxygen Minimum Zones (OMZs), which reportedly support phylogenetically diverse microbes. In this study, we aimed to characterize prokaryotic diversity in the water samples collected from 43, 200 and 1000 m depth of the Bay of Bengal Time Series location (BoBTS—18.0027°N, 89.0174°E) in the OMZ region. Illumina sequencing generated 3,921,854 reads of 16S rRNA gene amplicons, which corresponded to 5778 operational taxonomic units. The distribution of bacteria at class level varied with depth and oxygen concentration. α-Proteobacteria was found in abundance in 43 m and 1000 m depth water samples. γ-Proteobacteria was prominently detected in oxygen-depleted depths of 200 m and 1000 m. AB16 (Marine Group A, originally SAR406) was restricted at dissolved oxygen concentration of 1.5 μM at 200 m. Archaeal members were observed in low abundance (2%), with a high occurrence of phylum Euryarchaeota at 43 m, while Crenarchaeota was detected only at 200 m depth. Select bacterial cultures were screened for their ability to reduce nitrate in vitro, to obtain insights into their possible role in the nitrogen cycle. A total of 156 bacterial isolates clustered majorly with Alcanivorax, Bacillus, Erythrobacter, Halomonas, Idiomarina and Marinobacter. Among them, 11 bacterial genera showed positive nitrate reduction in the Griess test. A large percentage (63.55%) of 16S rRNA gene amplicons corresponded to unidentified OTUs at genus or higher taxonomic levels, suggesting a greater undiscovered prokaryotic diversity in this oxygen depleted region.


Bacteria High throughput sequencing Nitrate reducers North Indian Ocean 



The authors are thankful to Director, CSIR-NIO, and Head, Biological Oceanography Division for all the infrastructure and facilities. We are grateful to the Chief Scientists, Captains and Crew of the cruises SSD005 and SSD020. We thank Dr Damodar M. Shenoy from the Chemical Oceanography Division and anonymous reviewers for their valuable suggestions to improve the manuscript. The cruises were part of the SIBER program (GAP2425) funded by the Ministry of Earth Sciences (MoES), Government of India. CSIR India is acknowledged for funding the research through the PSC0108 (INDIAS IDEA) project. This publication has CSIR-NIO contribution number 6351.

Author Contributions

SD and BDS planned the work and was executed by GF and LM. GF was involved in sampling. RM has carried out the sequencing of the cultured isolates using in-house DNA sequencer. The results were analysed by SD, BDS, GF and LM. The manuscript was written and reviewed by SD, BDS, GF and LM.

Compliance with Ethical Standards

Conflict of interest

All authors declare that they have no conflict of interest.

Supplementary material

12088_2019_786_MOESM1_ESM.doc (496 kb)
Supplementary material 1 (DOC 496 kb)


  1. 1.
    Zinger L, Amaral-Zettler LA, Fuhrman JA, Horner-Devine MC, Huse SM, Welch DB, Martiny JB, Sogin M, Boetius A, Ramette A (2011) Global patterns of bacterial beta-diversity in seafloor and seawater ecosystems. PLoS ONE 6:e24570. CrossRefPubMedPubMedCentralGoogle Scholar
  2. 2.
    Nealson KH (1997) Sediment bacteria: Who’s there, what are they doing, and what’s new? Annu Rev Earth Planet Sci 25:403–434. CrossRefPubMedGoogle Scholar
  3. 3.
    Paulmier A, Ruiz-Pino D (2009) Oxygen minimum zones (OMZs) in the modern ocean. Prog Oceanogr 80:113–128. CrossRefGoogle Scholar
  4. 4.
    Bristow LA, Callbeck CM, Larsen M, Altabet MA, Dekaezemacker J, Forth M, Gauns M, Glud RN, Kuypers MM, Lavik G, Milucka J (2017) N2 production rates limited by nitrite availability in the Bay of Bengal oxygen minimum zone. Nat Geosci 10:24–29. CrossRefGoogle Scholar
  5. 5.
    Prasanna Kumar S, Nuncio M, Narvekar J, Kumar A, Sardesai S, De Souza SN, Gauns M, Ramaiah N, Madhupratap M (2004) Are eddies nature’s trigger to enhance biological productivity in the Bay of Bengal? Geophys Res Lett 31:L07309. CrossRefGoogle Scholar
  6. 6.
    Wright JJ, Konwar KM, Hallam SJ (2012) Microbial ecology of expanding oxygen minimum zones. Nat Rev Microbiol 10:381. CrossRefPubMedGoogle Scholar
  7. 7.
    Mulla A, Fernandes G, Menezes L, Meena RM, Naik H, Gauns M, Damare S (2017) Diversity of culturable nitrate-reducing bacteria from the Arabian Sea oxygen minimum zone. Deep-Sea Res Pt II 156:27–33. CrossRefGoogle Scholar
  8. 8.
    Vaz-Moreira I, Egas C, Nunes OC, Manaia CM (2011) Culture-dependent and culture-independent diversity surveys target different bacteria: a case study in a freshwater sample. Antonie van Leeuwenhoek J Microb 100:245–257. CrossRefGoogle Scholar
  9. 9.
    Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Pena AG, Goodrich JK, Gordon JI, Huttley GA (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:355–355. CrossRefPubMedPubMedCentralGoogle Scholar
  10. 10.
    Lane DJ (1999) 16S/23S rRNA sequencing. In: Stackebrandt E, Goodfellow M (eds) Nucleic acid techniques in bacterial systematics. Wiley, New York, pp 115–175Google Scholar
  11. 11.
    Stevens H, Ulloa O (2008) Bacterial diversity in the oxygen minimum zone of the eastern tropical South Pacific. Environ Microbiol 10:1244–1259. CrossRefPubMedGoogle Scholar
  12. 12.
    Rinke C, Schwientek P, Sczyrba A, Ivanova NN, Anderson IJ, Cheng JF, Darling A, Malfatti S, Swan BK, Gies EA, Dodsworth JA (2013) Insights into the phylogeny and coding potential of microbial dark matter. Nature 499:431–437. CrossRefPubMedGoogle Scholar
  13. 13.
    Hanshew AS, Mason CJ, Raffa KF, Currie CR (2013) Minimization of chloroplast contamination in 16S rRNA gene pyrosequencing of insect herbivore bacterial communities. J Microbiol Methods 95:149–155. CrossRefPubMedPubMedCentralGoogle Scholar
  14. 14.
    Zaikova E, Walsh DA, Stilwell CP, Mohn WW, Tortell PD, Hallam SJ (2010) Microbial community dynamics in a seasonally anoxic fjord: Saanich Inlet, British Columbia. Environ Microbiol 12:172–191. CrossRefPubMedGoogle Scholar
  15. 15.
    Bertagnolli AD, Padilla CC, Glass JB, Thamdrup B, Stewart FJ (2017) Metabolic potential and in situ activity of marine Marinimicrobia bacteria in an anoxic water column. Environ Microbiol 19:4392–4416. CrossRefPubMedGoogle Scholar
  16. 16.
    Bandekar M, Ramaiah N, Jain A, Meena RM (2018) Seasonal and depth-wise variations in bacterial and archaeal groups in the Arabian Sea oxygen minimum zone. Deep-Sea Res Part II 156:4–18. CrossRefGoogle Scholar
  17. 17.
    Canfield DE, Stewart FJ, Thamdrup B, De Brabandere L, Dalsgaard T, Delong EF, Revsbech NP, Ulloa O (2010) A cryptic sulfur cycle in oxygen minimum zone waters off the Chilean coast. Science 330:1375–1378. CrossRefPubMedGoogle Scholar
  18. 18.
    Mella-Flores D, Mazard S, Jeanthon C, Bendif EM, Ostrowski M, Scanlan DJ, Garczarek L, Humily F, Partensky F, Mahé F, Bariat L (2011) Is the distribution of Prochlorococcus and Synechococcus ecotypes in the Mediterranean Sea affected by global warming? Biogeosci Discuss 8:4281–4330. CrossRefGoogle Scholar
  19. 19.
    Campbell AM, Fleisher J, Sinigalliano C, White JR, Lopez JV (2015) Dynamics of marine bacterial community diversity of the coastal waters of the reefs, inlets, and wastewater outfalls of southeast Florida. Microbiologyopen 4:390–408. CrossRefPubMedPubMedCentralGoogle Scholar
  20. 20.
    Lamendella R, Strutt S, Borglin SE, Chakraborty R, Tas N, Mason OU, Hultman J, Prestat E, Hazen TC, Jansson J (2014) Assessment of the deepwater horizon oil spill impact on Gulf Coast microbial communities. Front Microbiol 5:1–13. CrossRefGoogle Scholar
  21. 21.
    Menezes LD, Fernandes GL, Mulla AB, Meena RM, Damare SR (2018) Diversity of culturable Sulphur-oxidising bacteria in the oxygen minimum zones of the northern Indian Ocean. J Mar Syst. CrossRefGoogle Scholar
  22. 22.
    Hugenholtz P (2002) Exploring prokaryotic diversity in the genomic era. Genome Biol 3:0003-1. CrossRefGoogle Scholar
  23. 23.
    Dell’Acqua S, Pauleta SR, Moura JJ, Moura I (2012) Biochemical characterization of the purple form of Marinobacter hydrocarbonoclasticus nitrous oxide reductase. Philos Trans R Soc B 367:1204–1212. CrossRefGoogle Scholar
  24. 24.
    Lalucat J, Bennasar A, Bosch R, Garcia-Valdes E, Palleroni NJ (2006) Biology of Pseudomonas stutzeri. Microbiol Mol Biol R 70:510–547. CrossRefGoogle Scholar

Copyright information

© Association of Microbiologists of India 2019

Authors and Affiliations

  1. 1.Biological Oceanography DivisionCSIR-National Institute of OceanographyDona PaulaIndia
  2. 2.Department of MicrobiologyGoa UniversityTaleigao PlateauIndia
  3. 3.CSIR-National Institute of Oceanography Regional CentreVisakhapatnamIndia

Personalised recommendations