Current Science

Open Access Open Access  Restricted Access Subscription Access

16s rRNA and Hydrazine Gene-Based Profiling of the Candidatus Scalindua Community from the Arabian Sea Hypoxic Sediments


Affiliations
1 Biological Oceanography Division, CSIR-National Institute of Oceanography, Goa 403 004, India
2 Academy of Scientific and Innovative Research, Ghaziabad 201 002, India
 

Anammox bacterial diversity and abundance were studied from the organic-rich hypoxic sediments of the Arabian Sea utilizing the partial 16S rRNA, and hydrazine synthase, hzsA and hydrazine oxidoreductase, hzo genes. Among all the clades obtained, phylotypic diversity was high within the Candidatus genus Scalindua with an abundance of ≤7 × 104 copies/g dry wt. As such, Scalindua is known to play a significant role in fixed nitrogen removal through anaerobic ammonium oxidation (anammox) pathway. From these analyses, it is inferred that searching for hzo gene yields robust evidence for detecting anammox community than the widely used 16S rRNA gene marker.

Keywords

Anammox, Community Gene-Based Profiling, Hydrazine, Hypoxic Sediments, Scalindua.
User
Notifications
Font Size

  • Lam, P. and Kuypers, M. M. M., Microbial nitrogen cycling processes in oxygen minimum zones. Annu. Rev. Mar. Sci., 2011, 3, 317–345.

  • Bulow, S. E., Rich, J. J., Naik, H. S., Pratihary, A. K. and Ward, B. B., Denitrification exceeds anammox as a nitrogen loss pathway in the Arabian Sea oxygen minimum zone. Deep-Sea Res. I: Oceanogr. Res., 2010, 57, 384–393.

  • Kuypers, M. M. et al., Massive nitrogen loss from the Benguela upwelling system through anaerobic ammonium oxidation. Proc. Natl. Acad. Sci. USA, 2005, 102, 6478–6483.

  • Kartal, B. et al., Molecular mechanism of anaerobic ammonium oxidation. Nature, 2011, 479, 127–130.

  • Harhangi, H. R. et al., Hydrazine synthase, a unique phylomarker with which to study the presence and biodiversity of anammox bacteria. Appl. Environ. Microbiol., 2012, 78, 752–758.

  • Dang, H., Zhou, H., Zhang, Z., Yu, Z., Hua, E., Liu, X. and Jiao, N., Molecular detection of Candidatus Scalindua pacifica and environmental responses of sediment anammox bacterial community in the Bohai Sea, China. PLoS ONE, 2013, 8, e61330.

  • Dalsgaard, T., Thamdrup, B. and Canfield, D. E., Anaerobic ammonium oxidation (anammox) in the marine environment. Res. Microbiol., 2005, 156, 457–464.

  • Griffiths, J. R. et al., The importance of benthic–pelagic coupling for marine ecosystem functioning in a changing world. Global Change Biol., 2017, 23, 2179–2196.

  • Barber, R. T. et al., Primary productivity and its regulation in the Arabian Sea during 1995. Deep-Sea Res. 2, 2001, 48(6–7), 1127–1172.

  • Van Mooy, B. A., Keil, R. G. and Devol, A. H., Impact of suboxia on sinking particulate organic carbon: enhanced carbon flux and preferential degradation of amino acids via denitrification. Geochim. Cosmochim. Acta, 2002, 66, 457–465.

  • Kalvelage, T. et al., Nitrogen cycling driven by organic matter export in the South Pacific oxygen minimum zone. Nature Geosci., 2013, 6, 228–234.

  • Jensen, M. M., Lam, P., Revsbech, N. P., Nagel, B., Gaye, B., Jetten, M. S. and Kuypers, M. M., Intensive nitrogen loss over the Omani Shelf due to anammox coupled with dissimilatory nitrite reduction to ammonium. ISME J., 2011, 5, 1660.

  • Strous, M. et al., Missing lithotroph identified as new planctomycete. Nature, 1999, 400, 446–449.

  • Schmid, M. et al., Molecular evidence for genus level diversity of bacteria capable of catalyzing anaerobic ammonium oxidation. Syst. Appl. Microbiol., 2000, 23, 93–106.

  • Schmid, M. et al., Candidatus ‘Scalindua brodae’, sp. Nov., candidatus ‘Scalindua wagneri’, sp. Nov., two new species of anaerobic ammonium oxidizing bacteria. Syst. Appl. Microbiol., 2003, 26, 529–538.

  • Kartal, B. et al., Candidatus ‘Anammoxoglobus propionicus’ a new propionate oxidizing species of anaerobic ammonium oxidizing bacteria. Syst. Appl. Microbiol., 2007, 30, 39–49.

  • Quan, Z. X. et al., Diversity of ammonium-oxidizing bacteria in a granular sludge anaerobic ammonium-oxidizing (anammox) reactor. Environ. Microbiol., 2008, 10, 3130–3139.

  • Viancelli, A. et al., Bacterial biodiversity from an anaerobic up flow bioreactor with anammox activity inoculated with swine sludge. Braz. Arch. Biol. Technol., 2011, 54, 1035–1041.

  • Khramenkov, S. et al., A novel bacterium carrying out anaerobic ammonium oxidation in a reactor for biological treatment of the filtrate of wastewater fermented sludge. Microbiology, 2013, 82, 628–636.

  • Sonthiphand, P., Hall, M. W. and Neufeld, J. D., Biogeography of anaerobic ammonia-oxidizing (anammox) bacteria. Front Microbiol., 2014, 5, 1–14.

  • Schmid, M. C. et al., Environmental detection of octahaem cytochrome c hydroxylamine/hydrazine oxidoreductase genes of aerobic and anaerobic ammonium-oxidizing bacteria. Environ. Microbiol., 2008, 10, 3140–3149.

  • Li, M. and Gu, J.-D., Advances in methods for detection of anaerobic ammonium oxidizing (anammox) bacteria. Appl. Microbiol. Biotechnol., 2011, 90, 1241.

  • Bhushan, R., Dutta, K. and Somayajulu, B., Concentrations and burial fluxes of organic and inorganic carbon on the eastern margins of the Arabian Sea. Mar. Geol., 2001, 178, 95–113.

  • Azam, F. and Sajjad, M. H., Colorimetric determination of organic carbon in soil by dichromate digestion in a microwave oven. PJBS, 2005, 8, 596–598.

  • Bernard, B. B., Bernard, H. and Brooks, J. M., Determination of total carbon, total organic carbon and inorganic carbon in sediments. TDI-Brooks International/B&B Labratories Inc, Texas, USA, 1995, pp. 1–5.

  • Nelson, D. and Sommers, L., Total carbon, organic carbon and organic matter. In Methods of Soil Analysis Part 2: Chemical and Microbiological Properties (ed. Page, A. L.), American Society of Agronomy, Soil Science Society of America, Madison (WI), USA, 1995, vol. 2, pp. 539–579.

  • Meyers, P. A., Preservation of elemental and isotopic source identification of sedimentary organic matter. Chem. Geol., 1994, 114, 289–302.

  • Plassart, P. et al., Evaluation of the iso standard 11063 DNA extraction procedure for assessing soil microbial abundance and community structure. PLoS ONE, 2012, 7, e44279.

  • Penton, C. R., Devol, A. H. and Tiedje, J. M., Molecular evidence for the broad distribution of anaerobic ammonium-oxidizing bacteria in freshwater and marine sediments. Appl. Environ. Microbiol., 2006, 72, 6829–6832.

  • Li, H., Chen, Shuo, Mu, Bo-Zhong and Gu, Ji-Dong, Molecular detection of anaerobic ammonium-oxidizing (anammox) bacteria in high-temperature petroleum reservoirs. Microb. Ecol., 2010, 60, 771–783.

  • Wang, S. et al., Comparative analysis of two 16S rRNA genebased pcr primer sets provides insight into the diversity distribution patterns of anammox bacteria in different environments. Appl. Microbiol. Biotechnol., 2015, 99, 8163–8176.

  • Kong, L., Jing, H., Kataoka, T., Buchwald, C. and Liu, H., Diversity and spatial distribution of hydrazine oxidoreductase (hzo) gene in the oxygen minimum zone off Costa Rica. PLoS ONE, 2013, 8, e78275.

  • Pitcher, A., Villanueva, L., Hopmans, E. C., Schouten, S., Reichart, G. J. and Damsté, J. S. S., Niche segregation of ammoniaoxidizing archaea and anammox bacteria in the Arabian Sea oxygen minimum zone. ISME J., 2011, 5, 1896–1904.

  • Bandekar, M., Ramaiah, N. and Meena, R. M., Diversity and abundance of denitrifying and anammox bacteria from the Arabian Sea oxygen minimum zone. Deep-Sea Res 2, 2018, 156, 19–26.

  • Jasmin, C. et al., Diversity of sediment-associated planctomycetes in the Arabian Sea oxygen minimum zone. J. Basic Microbiol., 2017, 57, 1010–1017.

  • Qian, G. et al., Diversity and distribution of anammox bacteria in water column and sediments of the eastern Indian Ocean. Int. Biodeterior. Biodegradation, 2018, 133, 52–62.

  • Yang, Y., Li, M., Li, X.-Y. and Gu, J.-D., Two identical copies of the hydrazine synthase gene clusters found in the genomes of anammox bacteria. Int. Biodeterior. Biodegr., 2018, 132, 236– 240.

  • Prasad, V., Garg, R., Singh, V. and Thakur, B., Organic matter distribution pattern in Arabian Sea: palynofacies analysis from the surface sediments off Karwar coast (West Coast of India). IJMS, 2007, 36, 399–406.

  • Nair, R. et al., Increased particle flux to the deep ocean related to monsoons. Nature, 1989, 338, 749.

  • Rabalais, N., Diaz, R. J., Levin, L., Turner, R., Gilbert, D. and Zhang, J., Dynamics and distribution of natural and human-caused hypoxia. Biogeosciences, 2010, 7, 585.

  • Escobar-Briones, E. and García-Villalobos, F. J., Distribution of total organic carbon and total nitrogen in deep-sea sediments from the southwestern Gulf of Mexico. Bol. Soc. Geol. Mex., 2009, 61, 73–86.

  • Sánchez, A., Distribution and composition of organic matter in sediments of the oxygen minimum zone of the northeastern Mexican Pacific: paleoceanographic implications/distribución y composición de la materia orgánica en sedimentos de la zona de oxígeno mínimo del pacífico nororiental mexicano: Implicaciones paleoceanográficas. J. Iber. Geol., 2013, 39, 111–120.

  • Paropkari, A. L., Babu, C. P. and Mascarenhas, A., A critical evaluation of depositional parameters controlling the variability of organic carbon in Arabian sea sediments. Mar. Geol., 1992, 107, 213–226.

  • Fu, L., Chen, Y., Li, S., He, H., Mi, T., Zhen, Y. and Yu, Z., Shifts in the anammox bacterial community structure and abundance in sediments from the changjiang estuary and its adjacent area. Syst. Appl. Microbiol., 2019, 42, 383–396.

  • Speth, D. R. and Jetten, M., Shotgun metagenomic data reveals significant abundance but low diversity of ‘Candidatus Scalindua’ marine anammox bacteria in the Arabian Sea oxygen minimum zone. Front. Microbiol., 2014, 5, 1–9.

  • Kuypers, M. M. et al., Anaerobic ammonium oxidation by anammox bacteria in the Black Sea. Nature, 2003, 422, 608–611.

  • Woebken, D. et al., A microdiversity study of anammox bacteria reveals a novel Candidatus Scalindua phylotype in marine oxygen minimum zones. Environ. Microbiol., 2008, 10, 3106–3119.

  • Hong, Y.-G., Li, M., Cao, H. and Gu, J.-D., Residence of habitatspecific anammox bacteria in the deep-sea subsurface sediments of the South China Sea: analyses of marker gene abundance with physical chemical parameters. Microb. Ecol., 2011, 62, 36–47.

  • Speth, D. R., Lagkouvardos, I., Wang, Y., Qian, P.-Y., Dutilh, B. E. and Jetten, M. S. M., Draft genome of Scalindua rubra, obtained from the interface above the discovery deep brine in the red sea, sheds light on potential salt adaptation strategies in anammox bacteria. Microb. Ecol., 2017, 74, 1–5.

  • Rich, J. J., Arevalo, P., Chang, B. X., Devol, A. H. and Ward, B. B., Anaerobic ammonium oxidation (anammox) and denitrification in Peru margin sediments. J. Mar. Syst., 2018, 207, 103–112.

  • Divya, B., Parvathi, A., Bharathi, P. L. and Nair, S., 16S rRNAbased bacterial diversity in the organic-rich sediments underlying oxygen-deficient waters of the eastern Arabian Sea. World J. Microbiol. Biotechnol., 2011, 27, 2821–2833.

  • Kumar, M., Daverey, A., Gu, J.-D. and Lin, J.-G., Anammox processes. In Current Developments in Biotechnology and Bioengineering (eds Larroche, C. M., Du, S. N. and Ashok Pandey, A.), Elsevier, The Netherlands, 2017, pp. 381–407.

  • Lipsewers, Y. A., Bale, N. J., Hopmans, E. C., Schouten, S., Sinninghe Damsté, J. S. and Villanueva, L., Seasonality and depth distribution of the abundance and activity of ammonia oxidizing microorganisms in marine coastal sediments (North Sea). Front Microbiol., 2014, 5, 1–12.

  • Bale, N. J., Villanueva, L., Fan, H., Stal, L. J., Hopmans, E. C., Schouten, S. and Sinninghe Damsté, J. S., Occurrence and activity of anammox bacteria in surface sediments of the southern North Sea. FEMS Microbiol. Ecol., 2014, 89, 99–110.

  • Kembel, S. W., Wu, M., Eisen, J. A. and Green, J. L., Incorporating 16S gene copy number information improves estimates of microbial diversity and abundance. PLoS Comput. Biol., 2012, 8, e1002743.

  • Strous, M. et al., Deciphering the evolution and metabolism of an anammox bacterium from a community genome. Nature, 2006, 440, 790.

  • Dietl, A. et al., The inner workings of the hydrazine synthase multiprotein complex. Nature, 2015, 527, 394.

  • Dang, H. et al., Environmental factors shape sediment anammox bacterial communities in hypernutrified Jiaozhou Bay, China. Appl. Environ. Microbiol., 2010, 76, 7036–7047.

  • Vieira, J. and Messing, J., The pUC plasmids, an M13mp7-derived system for insertion mutagenesis and sequencing with synthetic universal primers. Gene, 1982, 19, 259–268.


Abstract Views: 452

PDF Views: 114




  • 16s rRNA and Hydrazine Gene-Based Profiling of the Candidatus Scalindua Community from the Arabian Sea Hypoxic Sediments

Abstract Views: 452  |  PDF Views: 114

Authors

Jovitha Lincy
Biological Oceanography Division, CSIR-National Institute of Oceanography, Goa 403 004, India
Cathrine Sumathi Manohar
Academy of Scientific and Innovative Research, Ghaziabad 201 002, India

Abstract


Anammox bacterial diversity and abundance were studied from the organic-rich hypoxic sediments of the Arabian Sea utilizing the partial 16S rRNA, and hydrazine synthase, hzsA and hydrazine oxidoreductase, hzo genes. Among all the clades obtained, phylotypic diversity was high within the Candidatus genus Scalindua with an abundance of ≤7 × 104 copies/g dry wt. As such, Scalindua is known to play a significant role in fixed nitrogen removal through anaerobic ammonium oxidation (anammox) pathway. From these analyses, it is inferred that searching for hzo gene yields robust evidence for detecting anammox community than the widely used 16S rRNA gene marker.

Keywords


Anammox, Community Gene-Based Profiling, Hydrazine, Hypoxic Sediments, Scalindua.

References





DOI: https://doi.org/10.18520/cs%2Fv120%2Fi4%2F684-693