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Organic Matter Loading Modifies the Microbial Community Responsible for Nitrogen Loss in Estuarine Sediments

  • Microbiology of Aquatic Systems
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Abstract

Coastal marine sediments, as locations of substantial fixed nitrogen loss, are very important to the nitrogen budget and to the primary productivity of the oceans. Coastal sediment systems are also highly dynamic and subject to periodic natural and anthropogenic organic substrate additions. The response to organic matter by the microbial community involved in nitrogen loss processes was evaluated using mesocosms of Chesapeake Bay sediments. Over the course of a 50-day incubation, rates of anammox and denitrification were measured weekly using 15N tracer incubations, and samples were collected for genetic analysis. Rates of both nitrogen loss processes and gene abundances associated with them corresponded loosely, probably because heterogeneities in sediments obscured a clear relationship. The rates of denitrification were stimulated more, and the fraction of nitrogen loss attributed to anammox slightly reduced, by the higher organic matter addition. Furthermore, the large organic matter pulse drove a significant and rapid shift in the denitrifier community composition as determined using a nirS microarray, indicating that the diversity of these organisms plays an essential role in responding to anthropogenic inputs. We also suggest that the proportion of nitrogen loss due to anammox in these coastal estuarine sediments may be underestimated due to temporal dynamics as well as from methodological artifacts related to conventional sediment slurry incubation approaches.

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References

  1. Brandes JA, Devol AH (2002) A global marine-fixed nitrogen isotopic budget: implications for Holocene nitrogen cycling. Global Biogeochem Cycles 16:1120. doi:10.1029/2001GB001856

    Article  Google Scholar 

  2. Gruber N (2004) The dynamics of the marine nitrogen cycle and its influence on atmospheric CO2. In: Follows M, Oguz T (eds) The ocean carbon cycle and climate. Kluwer Academic, Dordrecht, pp 97–148

    Chapter  Google Scholar 

  3. Codispoti LA (2007) An oceanic fixed nitrogen sink exceeding 400 Tg N a−1 vs the concept of homeostasis in the fixed-nitrogen inventory. Biogeosciences 4:233–253. doi:10.5194/bgd-3-1203-2006

    Article  CAS  Google Scholar 

  4. Brandes JA, Devol AH (1997) Isotopic fractionation of oxygen and nitrogen in coastal marine sediments. Geochim Cosmochim Acta 61:1793–1801. doi:10.1016/S0016-7037(97)00041-0

    Article  CAS  Google Scholar 

  5. Babbin AR, Ward BB (2013) Controls on nitrogen loss processes in Chesapeake Bay sediments. Environ Sci Technol 47:4189–4196. doi:10.1021/es304842r

    Article  CAS  PubMed  Google Scholar 

  6. Glibert PM, Trice TM, Michael B, Lane L (2005) Urea in the tributaries of the Chesapeake and Coastal Bays of Maryland. Water Air Soil Pollut 160:229–243. doi:10.1007/s11270-005-2546-1

    Article  CAS  Google Scholar 

  7. Lomas MW, Trice TM, Glibert PM et al (2002) Temporal and spatial dynamics of urea uptake and regeneration rates and concentrations in Chesapeake Bay. Estuaries 25:469–482. doi:10.1007/BF02695988

    Article  CAS  Google Scholar 

  8. Glibert PM, Harrison J, Heil C, Seitzinger S (2006) Escalating worldwide use of urea—a global change contributing to coastal eutrophication. Biogeochemistry 77:441–463. doi:10.1007/s10533-005-3070-5

    Article  CAS  Google Scholar 

  9. Christensen PB, Rysgaard S, Sloth NP et al (2000) Sediment mineralization, nutrient fluxes, denitrification and dissimilatory nitrate reduction to ammonium in an estuarine fjord with sea cage trout farms. Aquat Microb Ecol 21:73–84. doi:10.3354/ame021073

    Article  Google Scholar 

  10. Lauer PR, Fernandez M, Fairweather PG et al (2009) Benthic fluxes of nitrogen and phosphorus at southern bluefin tuna Thunnus maccoyii sea-cages. Mar Ecol Prog Ser 390:251–263. doi:10.3354/meps08186

    Article  CAS  Google Scholar 

  11. Rich JJ, Dale OR, Song B, Ward BB (2008) Anaerobic ammonium oxidation (Anammox) in Chesapeake Bay sediments. Microb Ecol 55:311–320. doi:10.1007/s00248-007-9277-3

    Article  CAS  PubMed  Google Scholar 

  12. Koop-Jakobsen K, Giblin AE (2009) Anammox in tidal marsh sediments: the role of salinity, nitrogen loading, and marsh vegetation. Estuar Coasts 32:238–245. doi:10.1007/s12237-008-9131-y

    Article  CAS  Google Scholar 

  13. Braker G, Zhou J, Wu L et al (2000) Nitrite reductase genes (nirK and nirS) as functional markers to investigate diversity of denitrifying bacteria in Pacific Northwest marine sediment communities. Appl Environ Microbiol 66:2096–2104. doi:10.1128/AEM.66.5.2096-2104.2000

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Abell GCJ, Revill AT, Smith C et al (2009) Archaeal ammonia oxidizers and nirS-type denitrifiers dominate sediment nitrifying and denitrifying populations in a subtropical macrotidal estuary. ISME J 4:286–300. doi:10.1038/ismej.2009.105

    Article  PubMed  Google Scholar 

  15. Mosier AC, Francis CA (2010) Denitrifier abundance and activity across the San Francisco Bay estuary. Environ Microbiol Rep 2:667–676. doi:10.1111/j.1758-2229.2010.00156.x

    Article  CAS  PubMed  Google Scholar 

  16. Francis CA, O’Mullan GD, Cornwell JC, Ward BB (2013) Transitions in nirS-type denitrifier diversity, community composition, and biogeochemical activity along the Chesapeake Bay estuary. Front Microbiol 4:237. doi:10.3389/fmicb.2013.00237

    Article  PubMed  PubMed Central  Google Scholar 

  17. Bowen JL, Babbin AR, Kearns PJ, Ward BB (2014) Connecting the dots: linking nitrogen cycle gene expression to nitrogen fluxes in marine sediment mesocosms. Front Microbiol 5:429. doi:10.3389/fmicb.2014.00429

    Article  PubMed  PubMed Central  Google Scholar 

  18. Smith JM, Mosier AC, Francis CA (2015) Spatiotemporal relationships between the abundance, distribution, and potential activities of ammonia-oxidizing and denitrifying microorganisms in intertidal sediments. Microb Ecol 69:13–24. doi:10.1007/s00248-014-0450-1

    Article  CAS  PubMed  Google Scholar 

  19. Zimmerman AR, Canuel EA (2001) Bulk organic matter and lipid biomarker composition of Chesapeake Bay surficial sediments as indicators of environmental processes. Estuar Coast Shelf Sci 53:319–341. doi:10.1006/ecss.2001.0815

    Article  CAS  Google Scholar 

  20. Middelburg JJ, Soetaert K, Herman PMJ, Heip CHR (1996) Denitrification in marine sediments: a model study. Global Biogeochem Cycles 10:661–673. doi:10.1029/96GB02562

    Article  CAS  Google Scholar 

  21. Cornwell JC, Kemp WM, Kana TM (1999) Denitrification in coastal ecosystems: methods, environmental controls, and ecosystem level controls, a review. Aquat Ecol 33:41–54. doi:10.1023/A:1009921414151

    Article  CAS  Google Scholar 

  22. Naqvi SWA, Jayakumar DA, Narvekar PV et al (2000) Increased marine production of N2O due to intensifying anoxia on the Indian continental shelf. Nature 408:346–349. doi:10.1038/35042551

    Article  CAS  PubMed  Google Scholar 

  23. Dalsgaard T, Thamdrup B, Canfield DE (2005) Anaerobic ammonium oxidation (anammox) in the marine environment. Res Microbiol 156:457–464. doi:10.1016/j.resmic.2005.01.011

    Article  CAS  PubMed  Google Scholar 

  24. Engström P, Penton CR, Devol AH (2009) Anaerobic ammonium oxidation in deep-sea sediments off the Washington margin. Limnol Oceanogr 54:1643–1652. doi:10.4319/lo.2009.54.5.1643

    Article  Google Scholar 

  25. Castine SA, Erler DV, Trott LA et al (2012) Denitrification and anammox in tropical aquaculture settlement ponds: an isotope tracer approach for evaluating N2 production. PLoS One 7(9), e42810. doi:10.1371/journal.pone.0042810

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Minjeaud L, Michotey VD, Garcia N, Bonin PC (2009) Seasonal variation in di-nitrogen fluxes and associated processes (denitrification, anammox and nitrogen fixation) in sediment subject to shellfish farming influences. Aquat Sci 71:425–435. doi:10.1007/s00027-009-0100-8

    Article  CAS  Google Scholar 

  27. Lisa JA, Song B, Tobias CR, Duernberger KA (2014) Impacts of freshwater flushing on anammox community structure and activities in the New River Estuary, USA. Aquat Microb Ecol 72:17–31. doi:10.3354/ame01682

    Article  Google Scholar 

  28. Brin LD, Giblin AE, Rich JJ (2014) Environmental controls of anammox and denitrification in southern New England estuarine and shelf sediments. Limnol Oceanogr 59:851–860. doi:10.4319/lo.2014.59.3.0851

    Article  CAS  Google Scholar 

  29. Laanbroek HJ, Gerards S (1993) Competition for limiting amounts of oxygen between Nitrosomonas europaea and Nitrobacter winogradskyi grown in mixed continuous cultures. Arch Microbiol 159:453–459. doi:10.1007/BF00288593

    Article  CAS  Google Scholar 

  30. Kim J-G, Jung M-Y, Park S-J et al (2012) Cultivation of a highly enriched ammonia-oxidizing archaeon of thaumarchaeotal group I.1b from an agricultural soil. Environ Microbiol 14:1528–1543. doi:10.1111/j.1462-2920.2012.02740.x

    Article  CAS  PubMed  Google Scholar 

  31. Martens-Habbena W, Berube PM, Urakawa H et al (2009) Ammonia oxidation kinetics determine niche separation of nitrifying Archaea and Bacteria. Nature 461:976–979. doi:10.1038/nature08465

    Article  CAS  PubMed  Google Scholar 

  32. Thamdrup B, Dalsgaard T (2002) Production of N2 through anaerobic ammonium oxidation coupled to nitrate reduction in marine sediments. Appl Environ Microbiol 68:1312–1318. doi:10.1128/AEM.68.3.1312-1318.2002

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Bender M, Jahnke R, Weiss R et al (1989) Organic carbon oxidation and benthic nitrogen and silica dynamics in San Clemente Basin, a continental borderland site. Geochim Cosmochim Acta 53:685–697. doi:10.1016/0016-7037(89)90011-2

    Article  CAS  Google Scholar 

  34. Kemp WM, Sampou P, Caffrey J et al (1990) Ammonium recycling versus denitrification in Chesapeake Bay sediments. Limnol Oceanogr 35:1545–1563. doi:10.4319/lo.1990.35.7.1545

    Article  CAS  Google Scholar 

  35. Babbin AR, Keil RG, Devol AH, Ward BB (2014) Organic matter stoichiometry, flux, and oxygen control nitrogen loss in the ocean. Science 344:406–408. doi:10.1126/science.1248364

    Article  CAS  PubMed  Google Scholar 

  36. Trimmer M, Engstrom P (2011) Distribution, activity, and ecology of anammox bacteria in aquatic environments. In: Ward BB, Arp DJ, Klotz MG (eds) Nitrification. ASM Press, Washington, pp 201–235

    Chapter  Google Scholar 

  37. Dalsgaard T, Canfield DE, Petersen J et al (2003) N2 production by the anammox reaction in the anoxic water column of Golfo Dulce, Costa Rica. Nature 422:606–608. doi:10.1038/nature01526

    Article  CAS  PubMed  Google Scholar 

  38. Caffrey JM, Miller LG (1995) A comparison of two nitrification inhibitors used to measure nitrification rates in estuarine sediments. FEMS Microbiol Ecol 17:213–220. doi:10.1016/0168-6496(95)00026-7

    Article  CAS  Google Scholar 

  39. Newell RIE, Cornwell JC, Owens MS (2002) Influence of simulated bivalve biodeposition and microphytobenthos on sediment nitrogen dynamics: a laboratory study. Limnol Oceanogr 47:1367–1379. doi:10.4319/lo.2002.47.5.1367

    Article  Google Scholar 

  40. Hardison AK, Algar CK, Giblin AE, Rich JJ (2015) Influence of organic carbon and nitrate loading on partitioning between dissimilatory nitrate reduction to ammonium (DNRA) and N2 production. Geochim Cosmochim Acta 164:146–160. doi:10.1016/j.gca.2015.04.049

    Article  CAS  Google Scholar 

  41. Holmes RM, Aminot A, Kérouel R et al (1999) A simple and precise method for measuring ammonium in marine and freshwater ecosystems. Can J Fish Aquat Sci 56:1801–1808. doi:10.1139/f99-128

    Article  CAS  Google Scholar 

  42. Grasshoff K (1983) Determination of nitrite. In: Grasshoff K, Ehrhardt M, Kremling K (eds) Methods of seawater analysis, 2nd edn. Verlag Chemie, Weinheim, pp 143–150

    Google Scholar 

  43. Jayakumar A, O’Mullan GD, Naqvi SWA, Ward BB (2009) Denitrifying bacterial community composition changes associated with stages of denitrification in oxygen minimum zones. Microb Ecol 58:350–362. doi:10.1007/s00248-009-9487-y

    Article  CAS  PubMed  Google Scholar 

  44. Smith CJ, Nedwell DB, Dong LF, Osborn AM (2006) Evaluation of quantitative polymerase chain reaction-based approaches for determining gene copy and gene transcript numbers in environmental samples. Environ Microbiol 8:804–815. doi:10.1111/j.1462-2920.2005.00963.x

    Article  CAS  PubMed  Google Scholar 

  45. Ward BB, Bouskill NJ (2011) The utility of functional gene arrays for assessing community composition, relative abundance, and distribution of ammonia-oxidizing bacteria and archaea. Methods Enzymol 496:373–396. doi:10.1016/b978-0-12-386489-5.00015-4

    Article  CAS  PubMed  Google Scholar 

  46. Jayakumar A, Peng X, Ward BB (2013) Community composition of bacteria involved in fixed nitrogen loss in the water column of two major oxygen minimum zones in the ocean. Aquat Microb Ecol 70:245–259. doi:10.3354/ame01654

    Article  Google Scholar 

  47. Taroncher-Oldenburg G, Griner EM, Francis CA, Ward BB (2003) Oligonucleotide microarray for the study of functional gene diversity in the nitrogen cycle in the environment. Appl Environ Microbiol 69:1159–1171. doi:10.1128/AEM.69.2.1159-1171.2003

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Bulow SE, Francis CA, Jackson GA, Ward BB (2008) Sediment denitrifier community composition and nirS gene expression investigated with functional gene microarrays. Environ Microbiol 10:3057–3069. doi:10.1111/j.1462-2920.2008.01765.x

    Article  CAS  PubMed  Google Scholar 

  49. Peng X, Jayakumar A, Ward BB (2013) Community composition of ammonia-oxidizing archaea from surface and anoxic depths of oceanic oxygen minimum zones. Front Microbiol 4:177. doi:10.3389/fmicb.2013.00177

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Borcard D, Gillet F, Legendre P (2011) Numerical ecology with R. Springer, New York

    Book  Google Scholar 

  51. Strous M, Heijnen JJ, Kuenen JG, Jetten MSM (1998) The sequencing batch reactor as a powerful tool for the study of slowly growing anaerobic ammonium-oxidizing microorganisms. Appl Microbiol Biotechnol 50:589–596. doi:10.1007/s002530051340

    Article  CAS  Google Scholar 

  52. Van der Star WRL, van de Graaf MJ, Kartal B et al (2008) Response of anaerobic ammonium-oxidizing bacteria to hydroxylamine. Appl Environ Microbiol 74:4417–4426. doi:10.1128/AEM.00042-08

    Article  PubMed  PubMed Central  Google Scholar 

  53. Jayakumar DA, Francis CA, Naqvi SWA, Ward BB (2004) Diversity of nitrite reductase genes (nirS) in the denitrifying water column of the coastal Arabian Sea. Aquat Microb Ecol 34:69–78. doi:10.3354/ame034069

    Article  Google Scholar 

  54. Porubsky WP, Weston NB, Joye SB (2009) Benthic metabolism and the fate of dissolved inorganic nitrogen in intertidal sediments. Estuar Coast Shelf Sci 83:392–402. doi:10.1016/j.ecss.2009.04.012

    Article  CAS  Google Scholar 

  55. Algar CK, Vallino JJ (2014) Predicting microbial nitrate reduction pathways in coastal sediments. Aquat Microb Ecol 71:223–238. doi:10.3354/ame01678

    Article  Google Scholar 

  56. Kraft B, Tegetmeyer HE, Sharma R et al (2014) The environmental controls that govern the end product of bacterial nitrate respiration. Science 345:676–9. doi:10.1126/science.1254070

    Article  CAS  PubMed  Google Scholar 

  57. Behrendt A, Tarre S, Beliavski M et al (2014) Effect of high electron donor supply on dissimilatory nitrate reduction pathways in a bioreactor for nitrate removal. Bioresour Technol 171:291–297. doi:10.1016/j.biortech.2014.08.073

    Article  CAS  PubMed  Google Scholar 

  58. Stocker R (2012) Marine microbes see a sea of gradients. Science 338:628–633. doi:10.1126/science.1208929

    Article  CAS  PubMed  Google Scholar 

  59. Joye SB, Smith SV, Hollibaugh JT, Paerl HW (1996) Estimating denitrification rates in estuarine sediments: a comparison of stoichiometric and acetylene based methods. Biogeochemistry 33:197–215. doi:10.1007/BF02181072

    Article  CAS  Google Scholar 

  60. Teixeira C, Magalhäes C, Joye SB, Bordalo AA (2012) Potential rates and environmental controls of anaerobic ammonium oxidation in estuarine sediments. Aquat Microb Ecol 66:23–32. doi:10.3354/ame01548

  61. Song GD, Liu SM, Marchant H et al (2013) Anammox, denitrification and dissimilatory nitrate reduction to ammonium in the East China Sea sediment. Biogeosciences 10:6851–6864. doi:10.5194/bg-10-6851-2013

    Article  CAS  Google Scholar 

  62. Risgaard-Petersen N, Nicolaisen MH, Revsbech NP, Lomstein BA (2004) Competition between ammonia-oxidizing bacteria and benthic microalgae. Appl Environ Microbiol 70:5528–37. doi:10.1128/AEM.70.9.5528-5537.2004

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Trimmer M, Risgaard-Petersen N, Nicholls JC, Engström P (2006) Direct measurement of anaerobic ammonium oxidation (anammox) and denitrification in intact sediment cores. Mar Ecol Prog Ser 326:37–47. doi:10.3354/meps326037

    Article  CAS  Google Scholar 

  64. Van Kessel MAHJ, Harhangi HR, van de Pas-Schoonen K et al (2010) Biodiversity of N-cycle bacteria in nitrogen removing moving bed biofilters for freshwater recirculating aquaculture systems. Aquaculture 306:177–184. doi:10.1016/j.aquaculture.2010.05.019

    Article  Google Scholar 

  65. Matson EA, Brinson MM (1990) Stable carbon isotopes and the C:N ratio in the estuaries of the Pamlico and Neuse Rivers, North Carolina. Limnol Oceanogr 35:1290–1300. doi:10.4319/lo.1990.35.6.1290

    Article  CAS  Google Scholar 

  66. Law CS, Rees AP, Owens NJP (1991) Temporal variability of denitrification in estuarine sediments. Estuar Coast Shelf Sci 33:37–56. doi:10.1016/0272-7714(91)90069-N

    Article  CAS  Google Scholar 

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Acknowledgments

We thank J. Bowen, J. Cornwell, and M. Owens for assistance in obtaining sediments and site water from Chesapeake Bay and the UC Davis Stable Isotope Facility for their mass spectrometry measurements. O. Coyle assisted significantly in the sampling of the mesocosms and the tracer experiments. K. Farrell, D. Qiu, and N. Setlur assisted in the nutrient measurements. Funding was provided by a National Defense Science and Engineering Graduate Fellowship to ARB and National Science Foundation grants to BBW. This work was additionally funded by the Princeton Environmental Institute Siebel Energy Grand Challenges Initiative, and by an NSF Postdoctoral Fellowship to ARB (#1402109) during the writing of the manuscript.

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  1. Department of Geosciences, Princeton University, Princeton, NJ, USA

    Andrew R. Babbin, Amal Jayakumar & Bess B. Ward

  2. Department of Civil and Environmental Engineering, MIT, Cambridge, MA, USA

    Andrew R. Babbin

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Correspondence to Andrew R. Babbin.

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Babbin, A.R., Jayakumar, A. & Ward, B.B. Organic Matter Loading Modifies the Microbial Community Responsible for Nitrogen Loss in Estuarine Sediments. Microb Ecol 71, 555–565 (2016). https://doi.org/10.1007/s00248-015-0693-5

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