Anammox and Denitrification in the Intertidal Sediment of the Hypereutrophic Yatsu Tidal Flat, Japan
- 318 Downloads
An increase in available nitrogen loading in intertidal ecosystems causes eutrophication and macroalgae blooms. Denitrification and anaerobic ammonium oxidation (anammox) lead to the removal of bioavailable nitrogen, but few studies have examined this in intertidal sediments. The sediment anammox and denitrification rates in September 2015 and November 2016 were measured using a 15N tracer technique at two sites, with and without macroalgae, in the hypereutrophic Yatsu tidal flat, eastern Japan. At both sites, the rate of N2 production via anammox was consistently low compared with that via denitrification, accounting for < 7% of the total N2 production. In a fed-batch incubation experiment, the anammox rate increased in the surface sediment after 3 months. However, the contribution of anammox to nitrogen removal did not exceed that of denitrification, suggesting that denitrification is the major pathway for conversion of inorganic nitrogen to N2, and that anammox plays a limited role in nitrogen removal in the Yatsu tidal flat. Denitrification activity measured from August 2012 to January 2017 using the acetylene block method was higher in the sediment with macroalgae than that without. Multiple linear regression analysis revealed that denitrification in the sediment with macroalgae was limited by the nitrogen substrate, likely due to competition with macroalgae for nitrogen. Temperature and H2S production under macroalgae cover might also affect denitrification. In comparison, the organic carbon content was a key factor regulating heterotrophic denitrification in the sediment without macroalgae. These findings suggest that the occurrence of macroalgae changes the progress of denitrification in intertidal ecosystems.
KeywordsAnammox Denitrification Bioavailable inorganic nitrogen Intertidal ecosystem Eutrophication
We thank Kazuichi Isaka, Nobuyuki Aiko, and Kentaro Hayashi for their helpful discussion.
This work was supported by the Japan Society for the Promotion of Science KAKENHI, grant number JP15K00525.
- Amano, T., I. Yoshinaga, K. Okada, T. Yamagishi, S. Ueda, A. Obuchi, Y. Sako, and Y. Suwa. 2007. Detection of anammox activity and diversity of anammox bacteria-related 16S rRNA genes in coastal marine sediment in Japan. Microbes and Environments 22 (3): 232–242. https://doi.org/10.1264/jsme2.22.232.CrossRefGoogle Scholar
- Amano, T., I. Yoshinaga, T. Yamagishi, C.V. Thuoc, P.T. Thu, S. Ueda, K. Kato, Y. Sako, and Y. Suwa. 2011. Contribution of anammox bacteria to benthic nitrogen cycling in a mangrove forest and shrimp ponds, Haiphong, Vietnam. Microbes and Environments 26 (1): 1–6. https://doi.org/10.1264/jsme2.ME10150.CrossRefGoogle Scholar
- Bendschneider, K., and R.J. Robinson. 1952. A new spectrophotometric method for the determination of nitrite in sea water. Journal of Marine Research 11: 87–96.Google Scholar
- Capone, D.G., D.A. Bronk, M.R. Mulholland, and E.J. Carpenter. 2008. Nitrogen in the marine environment, 2nd edn. Estuaries. ISBN: 978-0-12-372522-6.Google Scholar
- De Brabandere, L., D.E. Canfield, T. Dalsgaard, G.E. Friederich, N.P. Revsbech, O. Ulloa, and B. Thamdrup. 2014. Vertical partitioning of nitrogen-loss processes across the oxic-anoxic interface of an oceanic oxygen minimum zone. Environmental Microbiology 16 (10): 3041–3051. https://doi.org/10.1111/1462-2920.12255.CrossRefGoogle Scholar
- Galloway, J.N., F.J. Dentener, D.G. Capone, E.W. Boyer, R.W. Howarth, S.P. Seitzinger, G.P. Asner, C.C. Cleveland, P.A. Green, E.A. Holland, D.M. Karl, A.F. Michaels, J.H. Porter, A.R. Townsend, and C.J. Vorosmarty. 2004. Nitrogen cycles: past, present, and future. Biogeochemistry 70 (2): 153–226. https://doi.org/10.1007/s10533-0040370-0.CrossRefGoogle Scholar
- Hou, L., Y. Zheng, M. Liu, J. Gong, X. Zhang, G. Yin, and L. You. 2013. Anaerobic ammonium oxidation (anammox) bacterial diversity, abundance, and activity in marsh sediments of the Yangtze estuary. Journal of Geophysical Research: Biogeosciences 118 (3): 1237–1246. https://doi.org/10.1002/jgrg.20108.CrossRefGoogle Scholar
- Howarth, R., F. Chan, D.J. Conley, J. Garnier, S.C. Doney, and R. Marino. 2011. Coupled biogeochemical cycles: eutrophication and hypoxia in temperate estuaries and coastal marine ecosystems. Frontiers in Ecology and the Environment 9 (1): 18–26. https://doi.org/10.1890/100008.CrossRefGoogle Scholar
- Isobe, K., Y. Suwa, J. Ikutani, M. Kuroiwa, T. Makita, Y. Takebayashi, M. Yoh, S. Otsuka, K. Senoo, M. Ohmori, and K. Koba. 2011. Analytical techniques for quantifying 15N/14N of nitrate, nitrite, total dissolved nitrogen and ammonium in environmental samples using a gas chromatograph equipped with a quadrupole mass spectrometer. Microbes and Environments 26 (1): 4653–4653. https://doi.org/10.1264/jsme2.ME10159.CrossRefGoogle Scholar
- Lam, P., and M.M.M. Kuypers. 2011. Microbial nitrogen cycling processes in oxygen minimum zones. Annual Review of Marine Science 3 (1): 317–345. https://doi.org/10.1146/annurev-marine-120709-142814.CrossRefGoogle Scholar
- Lisa, J.A., B. Song, C.R. Tobias, and D.E. Hines. 2015. Genetic and biogeochemical investigation of sedimentary nitrogen cycling communities responding to tidal and seasonal dynamics in Cape Fear River estuary. Estuarine, Coastal and Shelf Science 167: A313–A323. https://doi.org/10.1016/j.ecss.2015.09.008.CrossRefGoogle Scholar
- Lomstein, B.A., L.B. Guldberg, A.T.A. Neubauer, J. Hansen, A. Donnelly, R.A. Herbert, P. Viaroli, G. Giordani, R. Azzoni, R. de Wit, and K. Finster. 2006. Benthic decomposition of Ulva lactuca: a controlled laboratory experiment. Aquatic Botany 85 (4): 271–281. https://doi.org/10.1016/j.aquabot.2006.05.006.CrossRefGoogle Scholar
- Mulder, A., A.A. Vandegraaf, L.A. Robertson, and J.G. Kuenen. 1995. Anaerobic ammonium oxidation discovered in a denitrifying fluidized-bed reactor. FEMS Microbiology Ecology 16 (3): 177–183. https://doi.org/10.1111/j.1574-6941.1995.tb00281.x.CrossRefGoogle Scholar
- Nedergaard, R.I., N. Risgaard-Petersen, and K. Finster. 2002. The importance of sulfate reduction associated with Ulva lactuca thalli during decomposition: a mesocosm experiment. Journal of Experimental Marine Biology and Ecology 275 (1): 15–29. https://doi.org/10.1016/S0022-0981(02)00211-3.CrossRefGoogle Scholar
- Nielsen, L.P. 1992. Denitrification in sediment determined from nitrogen isotope pairing. FEMS Microbiology Ecology 86 (4): 357–362. https://doi.org/10.1111/j.1574-6968.1992.tb04828.x.CrossRefGoogle Scholar
- Payne, W.J. 1973. Reduction of nitrogenous oxides by microorganisms. Bacteriological Reviews 37 (4): 409–452.Google Scholar
- R Development Core Team 2015. R: a language and environment for statistical computing. Vienna: R Foundation for Statistical Computing. ISBN 3–900051–07-0, URL http://www.R-project.org.
- Sagi, T. 1966. Determination of ammonia in sea water by the indophenol method and its application to the coastal and off-shore waters. Oceanography Magagine 18: 43–51.Google Scholar
- Shiraki, Y., T. Kitazawa, S. Lee, and Y. Senga. 2018. A method for determining Batillaria attramentaria distribution using aerial balloon photography and a vegetation index camera: demonstration at the Yatsu tidal flat, Chiba Prefecture. Advances in Remote Sensing 7 (01): 15–24. https://doi.org/10.4236/ars.2018.71002.CrossRefGoogle Scholar
- Sørensen, J., J.M. Tiedje, and R.B. Firestone. 1980. Inhibition by sulfide of nitric and nitrous oxide reduction by denitrifying Pseudomonas fluorescens. Applied and Environmental Microbiology 39 (1): 105–108.Google Scholar
- Trimmer, M., D.B. Nedwell, D.B. Sivyer, and S.J. Malcolm. 2000. Seasonal organic mineralization and denitrification in intertidal sediments and their relationship to the abundance of Enteromorpha sp. and Ulva sp. Marine Ecology Progress Series 203: 67–80. https://doi.org/10.3354/meps203067.CrossRefGoogle Scholar
- van de Graaf, A.A., A. Mulder, P. Debruijn, M.S.M. Jetten, L.A. Robertson, and J.G. Kuenen. 1995. Anaerobic oxidation of ammonium is a biologically mediated process. Applied and Environmental Microbiology 61 (4): 1246–1251.Google Scholar
- Wetzel, P.G. 2001. 23 Detritus: organic carbon cycling and ecosystem metabolism. In Limnology, lake and river ecosystems, 731–783. Elsevier Inc.Google Scholar
- Yoshimura, M., and S. Yamochi. 2011. Research on the seasonal succession of green tide and tolerance of a causative seaweed Ulva ohnoi to low salinity and desiccation at the north pond of Osaka Nanko Bird Sanctuary (In Japanese, with English abstract). 67:I_1136–I_1140. https://doi.org/10.2208/kaigan.67.I_1136.
- Yoshinaga, I., T. Amano, T. Yamagishi, K. Okada, S. Ueda, Y. Sako, and Y. Suwa. 2011. Distribution and diversity of anaerobic ammonium oxidation (anammox) bacteria in the sediment of a eutrophic freshwater lake, Lake Kitaura, Japan. Microbes and Environments 26 (3): 189–197. https://doi.org/10.1264/jsme2.ME10184.CrossRefGoogle Scholar