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Ecosystems

, Volume 22, Issue 4, pp 912–928 | Cite as

Saltwater Intrusion Modifies Microbial Community Structure and Decreases Denitrification in Tidal Freshwater Marshes

  • Scott C. NeubauerEmail author
  • Michael F. Piehler
  • Ashley R. Smyth
  • Rima B. Franklin
Article

Abstract

Environmental changes can alter the interactions between biotic and abiotic ecosystem components in tidal wetlands and therefore impact important ecosystem functions. The objective of this study was to determine how saltwater intrusion affects wetland nutrient biogeochemistry, with a specific focus on the soil microbial communities and physicochemical parameters that control nitrate removal. Our work took place in a tidal freshwater marsh in South Carolina, USA, where a 3.5-year saltwater intrusion experiment increased porewater salinities from freshwater to oligohaline levels. We measured rates of denitrification, soil oxygen demand, and dissimilatory nitrate reduction to ammonium (DNRA) and used molecular genetic techniques to assess the abundance and community structure of soil microbes. In soils exposed to elevated salinities, rates of denitrification were reduced by about 70% due to changes in the soil physicochemical environment (higher salinity, higher carbon:nitrogen ratio) and shifts in the community composition of denitrifiers. Saltwater intrusion also affected the microbial community responsible for DNRA, increasing the abundance of genes associated with this process and shifting microbial community composition. Though rates of DNRA were below detection, the microbial community response may be a precursor to increased rates of DNRA with continued saltwater intrusion. Overall, saltwater intrusion reduces the ability of tidal freshwater marshes to convert reactive nitrogen to dinitrogen gas and therefore negatively affects their water quality functions. Continued study of the interrelationships between biotic communities, the abiotic environment, and biogeochemical transformations will lead to a better understanding of how the progressive replacement of tidal freshwater marshes with brackish analogues will affect the overall functioning of the coastal landscape.

Keywords

ecosystem ecology global change nitrogen cycle salinization sea level rise wetland 

Notes

Acknowledgements

We thank Rebecca Schwartz and Amanda Rotella for excellent field assistance, especially in maintaining the field salinity manipulation experiment and collecting the soil cores analyzed herein. Additionally, we offer sincere thanks to Wayne Gardner, Liana Nichols, Suzanne Thompson, Gabriella Balasa, and David Berrier for their invaluable roles in this project. We are also grateful to Bob Jewell and the staff of Brookgreen Gardens. Without their permission to access the site, this research would not have been possible. We also acknowledge the efforts of two anonymous reviewers, whose comments helped improve the manuscript. This research was primarily supported by grants to S.C.N. from the University of South Carolina, Office of Research and Health Sciences Research Funding Program, and the US Department of Energy’s Office of Science (BER) through the Coastal Center of the National Institute for Climatic Change Research at Tulane University (DOE Grant # DE-FC02-06ER64298). Additional support was provided by the National Science Foundation (NSF EAR-0815627 to M.F.P. and NSF DEB-1355059 to R.B.F. and S.C.N.). This is contribution #1868 from the University of South Carolina’s Belle W. Baruch Institute for Marine and Coastal Sciences.

References

  1. An S, Gardner WS. 2002. Dissimilatory nitrate reduction to ammonium (DNRA) as a nitrogen link, versus denitrification as a sink in a shallow estuary (Laguna Madre/Baffin Bay, Texas). Mar Ecol Prog Ser 237:41–50.CrossRefGoogle Scholar
  2. An S, Joye SB. 2001. Enhancement of coupled nitrification-denitrification by benthic photosynthesis in shallow estuarine sediments. Limnol Oceanogr 46:62–74.CrossRefGoogle Scholar
  3. Ardón M, Morse JL, Colman BP, Bernhardt ES. 2013. Drought-induced saltwater incursion leads to increased wetland nitrogen export. Glob Change Biol 19:2976–85.  https://doi.org/10.1111/gcb.12287.CrossRefGoogle Scholar
  4. Azziz G, Monza J, Etchebehere C, Irisarri P. 2017. nirS- and nirK-type denitrifier communities are differentially affected by soil type, rice cultivar and water management. Eur J Soil Biol 78:20–8.  https://doi.org/10.1016/j.ejsobi.2016.11.003.CrossRefGoogle Scholar
  5. Babbin AR, Jayakumar A, Ward BB. 2016. Organic matter loading modifies the microbial community responsible for nitrogen loss in estuarine sediments. Microb Ecol 71:555–65.  https://doi.org/10.1007/s00248-015-0693-5.CrossRefPubMedGoogle Scholar
  6. Borsuk ME, Higdon D, Stow CA, Reckhow KH. 2001. A Bayesian hierarchical model to predict benthic oxygen demand from organic matter loading in estuaries and coastal zones. Ecol Modell 143:165–81.CrossRefGoogle Scholar
  7. 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.  https://doi.org/10.3389/fmicb.2014.00429.CrossRefPubMedPubMedCentralGoogle Scholar
  8. Braker G, Zhou J, Wu L, Devol AH, Tiedje JM. 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 66:2096–104.  https://doi.org/10.1128/AEM.66.5.2096-2104.2000.CrossRefPubMedPubMedCentralGoogle Scholar
  9. Brunet RC, Garcia-Gil LJ. 1996. Sulfide-induced dissimilatory nitrate reduction to ammonia in anaerobic freshwater sediments. FEMS Microbiol Ecol 21:131–8.CrossRefGoogle Scholar
  10. Burgin AJ, Hamilton SK. 2007. Have we overemphasized the role of denitrification in aquatic ecosystems? A review of nitrate removal pathways. Front Ecol Environ 5:89–96.  https://doi.org/10.1890/1540-9295(2007)5[89:HWOTRO]2.0.CO;2.CrossRefGoogle Scholar
  11. Caffrey JM, Sloth NP, Kaspar HF, Blackburn TH. 1993. Effect of organic loading on nitrification and denitrification in a marine sediment microcosm. FEMS Microbiol Ecol 12:159–67.CrossRefGoogle Scholar
  12. Chambers LG, Osborne TZ, Reddy KR. 2013. Effect of salinity-altering pulsing events on soil organic carbon loss along an intertidal wetland gradient: a laboratory experiment. Biogeochemistry .  https://doi.org/10.1007/s10533-013-9841-5.CrossRefGoogle Scholar
  13. Craft C, Clough J, Ehman J, Joye S, Park R, Pennings S, Guo H, Machmuller M. 2009. Forecasting the effects of accelerated sea-level rise on tidal marsh ecosystem services. Front Ecol Environ 7:73–8.  https://doi.org/10.1890/070219.CrossRefGoogle Scholar
  14. Cytryn E, Minz D, Oremland RS, Cohen Y. 2000. Distribution and diversity of Archaea corresponding to the limnological cycle of a hypersaline stratified lake (Solar Lake, Sinai, Egypt). Appl Environ Microbiol 66:3269–76.  https://doi.org/10.1128/AEM.66.8.3269-3276.2000.CrossRefPubMedPubMedCentralGoogle Scholar
  15. DeLaune RD, Nyman JA, Patrick WH Jr. 1994. Peat collapse, ponding, and wetland loss in a rapidly submerging coastal marsh. J Coast Res 10:1021–30.Google Scholar
  16. Dodla SK, Wang JJ, DeLaune RD, Cook RL. 2008. Denitrification potential and its relation to organic carbon quality in three coastal wetland soils. Sci Total Environ 407:471–80.  https://doi.org/10.1016/j.scitotenv.2008.08.022.CrossRefGoogle Scholar
  17. Edmonds JW, Weston NB, Joye SB, Mou X, Moran MA. 2009. Microbial community response to seawater amendment in low-salinity tidal sediments. Microb Ecol 58:558–68.  https://doi.org/10.1007/s00248-009-9556-2.CrossRefPubMedGoogle Scholar
  18. Ensign SH, Piehler MF, Doyle MW. 2008. Riparian zone denitrification affects nitrogen flux through a tidal freshwater river. Biogeochemistry 91:133–50.  https://doi.org/10.1007/s10533-008-9265-9.CrossRefGoogle Scholar
  19. Enwall K, Throbäck IN, Stenberg M, Söderström M, Hallin S. 2010. Soil resources influence spatial patterns of denitrifying communities at scales compatible with land management. Appl Environ Microbiol 76:2243–50.CrossRefPubMedPubMedCentralGoogle Scholar
  20. Eyre BD, Rysgaard S, Dalsgaard T, Christensen PB. 2002. Comparison of isotope pairing and N2:Ar methods for measuring sediment denitrification—assumptions, modifications, and implications. Estuaries 25:1077–87.CrossRefGoogle Scholar
  21. Fennel K, Brady D, DiToro D, Fulweiler RW, Gardner WS, Giblin A, McCarthy MJ, Rao A, Seitzinger S, Thouvenot-Korppoo M, Tobias C. 2009. Modeling denitrification in aquatic sediments. Biogeochemistry 93:159–78.  https://doi.org/10.1007/s10533-008-9270-z.CrossRefGoogle Scholar
  22. Foulquier A, Volat B, Neyra M, Bornette G, Montuelle B. 2013. Long-term impact of hydrological regime on structure and functions of microbial communities in riverine wetland sediments. FEMS Microbiol Ecol 85:211–26.CrossRefPubMedGoogle Scholar
  23. Franklin RB, Morrissey EM, Morina JC. 2017. Changes in abundance and community structure of nitrate-reducing bacteria along a salinity gradient in tidal wetlands. Pedobiologia 60:21–6.  https://doi.org/10.1016/j.pedobi.2016.12.002.CrossRefGoogle Scholar
  24. Gardner WS, Bootsma HA, Evans C, John PAS. 1995. Improved chromatographic analysis of 15 N:14 N ratios in ammonium or nitrate for isotope addition experiments. Mar Chem 48:271–82.CrossRefGoogle Scholar
  25. Gardner WS, McCarthy MJ. 2009. Nitrogen dynamics at the sediment–water interface in shallow, sub-tropical Florida Bay: why denitrification efficiency may decrease with increased eutrophication. Biogeochemistry 95:185–98.CrossRefGoogle Scholar
  26. Gardner WS, McCarthy MJ, An S, Sobolev D, Sell KS, Brock D. 2006. Nitrogen fixation and dissimilatory nitrate reduction to ammonium (DNRA) support nitrogen dynamics in Texas estuaries. Limnol Oceanogr 51:558–68.  https://doi.org/10.4319/lo.2006.51.1_part_2.0558.CrossRefGoogle Scholar
  27. Giblin AE, Weston NB, Banta GT, Tucker J, Hopkinson CS. 2010. The effects of salinity on nitrogen losses from an oligohaline estuarine sediment. Estuaries Coast 33:1054–68.CrossRefGoogle Scholar
  28. Greene SE. 2005. Nutrient removal by tidal fresh and oligohaline marshes in a Chesapeake Bay tributary. M.S. thesis, University of Maryland, College Park, MD.Google Scholar
  29. Gribsholt B, Boschker HTS, Struyf E, Andersson M, Tramper A, De Brabandere L, van Damme S, Brion N, Meire P, Dehairs F, Middelburg JJ, Heip CHR. 2005. Nitrogen processing in a tidal freshwater marsh: A whole-ecosystem 15N labeling study. Limnol Oceanogr 50:1945–59.CrossRefGoogle Scholar
  30. Hackney CT, Avery GB, Leonard LA, Posey M, Aplhin T. 2007. Biological, chemical, and physical characteristics of tidal freshwater swamp forests of the Lower Cape Fear River/Estuary, North Carolina. In: Conner WH, Doyle TW, Krauss KW, Eds. Ecology of tidal freshwater forested wetlands of the Southeastern United States. The Netherlands: Springer. p 183–221.CrossRefGoogle Scholar
  31. Hamersley MR. 2002. The role of denitrification in the nitrogen cycle of New England salt marshes. Ph.D. dissertation, Massachusetts Institute of Technology, Cambridge, MA and the Woods Hole Oceanographic Institution, Woods Hole, MA.Google Scholar
  32. Hammer Ø. 2001. PAST: Paleontological statistics software package for education and data analysis. Palaeontologica Electronica 4:1–9.Google Scholar
  33. Herbert ER, Boon P, Burgin AJ, Neubauer SC, Franklin RB, Ardón M, Hopfensperger KN, Lamers LPM, Gell P. 2015. A global perspective on wetland salinization: Ecological consequences of a growing threat to freshwater wetlands. Ecosphere 6:art206.  https://doi.org/10.1890/es14-00534.1.
  34. Herbert ER, Schubauer-Berigan J, Craft CB. 2018. Differential effects of chronic and acute simulated seawater intrusion on tidal freshwater marsh carbon cycling. Biogeochemistry 138:137–54.  https://doi.org/10.1007/s10533-018-0436-z.CrossRefGoogle Scholar
  35. Hobbie JE. 1988. A comparison of the ecology of planktonic bacteria in fresh and salt water. Limnol Oceanogr 33:750–64.Google Scholar
  36. Hochard S, Pinazo C, Grenz C, Evans JLB, Pringault O. 2010. Impact of microphytobenthos on the sediment biogeochemical cycles: a modeling approach. Ecol Modell 221:1687–701.CrossRefGoogle Scholar
  37. Hopfensperger KN, Kaushal SS, Findlay SEG, Cornwell JC. 2009. Influence of plant communities on denitrification in a tidal freshwater marsh of the Potomac River, United States. J Environ Qual 38:618.  https://doi.org/10.2134/jeq2008.0220.CrossRefPubMedGoogle Scholar
  38. Hume NP, Fleming MS, Horne AJ. 2002. Denitrification potential and carbon quality of four aquatic plants in wetland microcosms. Soil Sci Soc Am J 66:1706.  https://doi.org/10.2136/sssaj2002.1706.CrossRefGoogle Scholar
  39. Jackson CR, Vallaire SC. 2009. Effects of salinity and nutrients on microbial assemblages in Louisiana wetland sediments. Wetlands 29:277–87.CrossRefGoogle Scholar
  40. Jones CM, Hallin S. 2010. Ecological and evolutionary factors underlying global and local assembly of denitrifier communities. ISME J 4:633–41.  https://doi.org/10.1038/ismej.2009.152.CrossRefPubMedGoogle Scholar
  41. Jordan TE, Cornwell JC, Boynton WR, Anderson JT. 2008. Changes in phosphorus biogeochemistry along an estuarine salinity gradient: the iron conveyer belt. Limnol Oceanogr 53:172–84.  https://doi.org/10.4319/lo.2008.53.1.0172.CrossRefGoogle Scholar
  42. Joye SB, Hollibaugh JT. 1995. Influence of sulfide inhibition of nitrification on nitrogen regeneration in sediments. Science 270:623–5.CrossRefGoogle Scholar
  43. Jun M, Altor AE, Craft CB. 2013. Effects of increased salinity and inundation on inorganic nitrogen exchange and phosphorus sorption by tidal freshwater floodplain forest soils, Georgia (USA). Estuaries Coast 36:508–18.  https://doi.org/10.1007/s12237-012-9499-6.CrossRefGoogle Scholar
  44. Kana TM, Darkangelo C, Hunt MD, Oldham JB, Bennett GE, Cornwell JC. 1994. Membrane inlet mass spectrometer for rapid high-precision determination of N2, O2, and Ar in environmental water samples. Anal Chem 66:4166–70.  https://doi.org/10.1021/ac00095a009.CrossRefGoogle Scholar
  45. Koch MS, Mendelssohn IA, McKee KL. 1990. Mechanism for the hydrogen sulphide-induced growth limitation in wetland macrophytes. Limnol Oceanogr 35:399–408.CrossRefGoogle Scholar
  46. Koop-Jakobsen K, Giblin AE. 2009. Anammox in tidal marsh sediments: the role of salinity, nitrogen loading, and marsh vegetation. Estuaries Coast 32:238–45.  https://doi.org/10.1007/s12237-008-9131-y.CrossRefGoogle Scholar
  47. Kostka JE, Luther GWIII. 1995. Seasonal cycling of Fe in salt marsh sediments. Biogeochemistry 29:159–81.CrossRefGoogle Scholar
  48. Lane DI. 1991. 16S/23S sequencing. In: Stackebrandt E, Goodfellow M, Eds. Nucleic acid techniques in bacterial systematics. New York: Wiley. p 115–76.Google Scholar
  49. Lavrentyev PJ, Gardner WS, Yang L. 2000. Effects of the zebra mussel on nitrogen dynamics and the microbial community at the sediment-water interface. Aquat Microb Ecol 21:187–94.CrossRefGoogle Scholar
  50. Lisa JA, Song B, Tobias CR, Hines DE. 2015. Genetic and biogeochemical investigation of sedimentary nitrogen cycling communities responding to tidal and seasonal dynamics in Cape Fear River Estuary. Estuar Coast Shelf Sci 167, Part:A313–23.  https://doi.org/10.1016/j.ecss.2015.09.008.
  51. Magalhães CM, Joye SB, Moreira RM, Wiebe WJ, Bordalo AA. 2005. Effect of salinity and inorganic nitrogen concentrations on nitrification and denitrification rates in intertidal sediments and rocky biofilms of the Douro River estuary, Portugal. Water Res 39:1783–94.  https://doi.org/10.1016/j.watres.2005.03.008.CrossRefPubMedGoogle Scholar
  52. Marton JM, Herbert ER, Craft CB. 2012. Effects of salinity on denitrification and greenhouse gas production from laboratory-incubated tidal forest soils. Wetlands 32:347–57.  https://doi.org/10.1007/s13157-012-0270-3.CrossRefGoogle Scholar
  53. McGlathery KJ, Sundbäck K, Anderson IC. 2007. Eutrophication in shallow coastal bays and lagoons: The role of plants in the coastal filter. Mar Ecol Prog Ser 348:1–18.  https://doi.org/10.3354/meps07132.CrossRefGoogle Scholar
  54. Merrill JZ. 1999. Tidal freshwater marshes as nutrient sinks: particulate nutrient burial and denitrification. M.S. thesis, University of Maryland, College Park, MD.Google Scholar
  55. Miller-Way T, Twilley RR. 1996. Theory and operation of continuous flow systems for the study of benthic-pelagic coupling. Mar Ecol Prog Ser 140:257–69.CrossRefGoogle Scholar
  56. Morrissey EM, Berrier DJ, Neubauer SC, Franklin RB. 2014. Using microbial communities and extracellular enzymes to link soil organic matter characteristics to greenhouse gas production in a tidal freshwater wetland. Biogeochemistry 117:473–90.  https://doi.org/10.1007/s10533-013-9894-5.CrossRefGoogle Scholar
  57. Morrissey EM, Franklin RB. 2015. Resource effects on denitrification are mediated by community composition in tidal freshwater wetlands soils. Environ Microbiol 17:1520–32.  https://doi.org/10.1111/1462-2920.12575.CrossRefPubMedGoogle Scholar
  58. Morrissey EM, Jenkins AS, Brown BL, Franklin RB. 2013. Resource availability effects on nitrate-reducing microbial communities in a freshwater wetland. Wetlands 33:301–10.  https://doi.org/10.1007/s13157-013-0384-2.CrossRefGoogle Scholar
  59. Mosier AC, Francis CA. 2010. Denitrifier abundance and activity across the San Francisco Bay estuary. Environ Microbiol Rep 2:667–76.  https://doi.org/10.1111/j.1758-2229.2010.00156.x.CrossRefPubMedGoogle Scholar
  60. Munns R, Tester M. 2008. Mechanisms of salinity tolerance. Annu Rev Plant Biol 59:651–81.  https://doi.org/10.1146/annurev.arplant.59.032607.092911.CrossRefGoogle Scholar
  61. Murphy AE, Anderson IC, Smyth AR, Song B, Luckenbach MW. 2016. Microbial nitrogen processing in hard clam (Mercenaria mercenaria) aquaculture sediments: the relative importance of denitrification and dissimilatory nitrate reduction to ammonium (DNRA). Limnol Oceanogr 61:1589–604.CrossRefGoogle Scholar
  62. Nelson TM, Streten C, Gibb KS, Chariton AA. 2015. Saltwater intrusion history shapes the response of bacterial communities upon rehydration. Sci Total Environ 502:143–8.  https://doi.org/10.1016/j.scitotenv.2014.08.109.CrossRefPubMedGoogle Scholar
  63. Neubauer SC. 2013. Ecosystem responses of a tidal freshwater marsh experiencing saltwater intrusion and altered hydrology. Estuaries Coast 36:491–507.  https://doi.org/10.1007/s12237-011-9455-x.CrossRefGoogle Scholar
  64. Neubauer SC, Franklin RB, Berrier DJ. 2013. Saltwater intrusion into tidal freshwater marshes alters the biogeochemical processing of organic carbon. Biogeosciences 10:8171–83.  https://doi.org/10.5194/bg-10-8171-2013.CrossRefGoogle Scholar
  65. Noe GB, Krauss KW, Lockaby BG, Conner WH, Hupp CR. 2012. The effect of increasing salinity and forest mortality on soil nitrogen and phosphorus mineralization in tidal freshwater forested wetlands. Biogeochemistry .  https://doi.org/10.1007/s10533-012-9805-1.CrossRefGoogle Scholar
  66. Nyman JA, DeLaune RD, Roberts HH, Patrick WH Jr. 1993. Relationship between vegetation and soil formation in a rapidly submerging coastal marsh. Mar Ecol Prog Ser 96:269–79.CrossRefGoogle Scholar
  67. Osborne RI, Bernot MJ, Findlay SEG. 2015. Changes in nitrogen cycling processes along a salinity gradient in tidal wetlands of the Hudson River, New York, USA. Wetlands 35:323–34.  https://doi.org/10.1007/s13157-014-0620-4.CrossRefGoogle Scholar
  68. Perry JE, Hershner C. 1999. Temporal changes in the vegetation pattern in a tidal freshwater marsh. Wetlands 19:90–9.CrossRefGoogle Scholar
  69. Philippot L, Spor A, Hénault C, Bru D, Bizouard F, Jones CM, Sarr A, Maron PA. 2013. Loss in microbial diversity affects nitrogen cycling in soil. ISME J 7:1609–19.CrossRefPubMedPubMedCentralGoogle Scholar
  70. Piehler MF, Smyth AR. 2011. Habitat-specific distinctions in estuarine denitrification affect both ecosystem function and services. Ecosphere 2:art12.  https://doi.org/10.1890/es10-00082.1.
  71. Plummer P, Tobias C, Cady D. 2015. Nitrogen reduction pathways in estuarine sediments: influences of organic carbon and sulfide. J Geophys Res Biogeosci 120:1958–72.  https://doi.org/10.1002/2015JG003057.CrossRefGoogle Scholar
  72. Reeburgh WS. 1969. Observations of gases in Chesapeake Bay sediments. Limnol Oceanogr 14:368–75.CrossRefGoogle Scholar
  73. Reed HE, Martiny JBH. 2012. Microbial composition affects the functioning of estuarine sediments. ISME J 7:868–79.CrossRefPubMedPubMedCentralGoogle Scholar
  74. Santoro AE, Boehm AB, Francis CA. 2006. Denitrifier community composition along a nitrate and salinity gradient in a coastal aquifer. Appl Environ Microbiol 72:2102–9.  https://doi.org/10.1128/AEM.72.3.2102-2109.2006.CrossRefPubMedPubMedCentralGoogle Scholar
  75. Schoepfer VA, Bernhardt ES, Burgin AJ. 2014. Iron clad wetlands: soil iron-sulfur buffering determines coastal wetland response to salt water incursion. J Geophys Res Biogeosci 119:2209–19.  https://doi.org/10.1002/2014JG002739.CrossRefGoogle Scholar
  76. Scott JT, McCarthy MJ, Gardner WS, Doyle RD. 2008. Denitrification, dissimilatory nitrate reduction to ammonium, and nitrogen fixation along a nitrate concentration gradient in a created freshwater wetland. Biogeochemistry 87:99–111.  https://doi.org/10.1007/s10533-007-9171-6.CrossRefGoogle Scholar
  77. Seitzinger SP, Gardner WS, Spratt AK. 1991. The effect of salinity on ammonium sorption in aquatic sediments—implications for benthic nutrient recycling. Estuaries 14:167–74.CrossRefGoogle Scholar
  78. Seldomridge ED, Prestegaard KL. 2012. Use of geomorphic, hydrologic, and nitrogen mass balance data to model ecosystem nitrate retention in tidal freshwater wetlands. Biogeosciences 9:2661–72.  https://doi.org/10.5194/bg-9-2661-2012.CrossRefGoogle Scholar
  79. Senga Y, Mochida K, Fukumori R, Okamoto N, Seike Y. 2006. N2O accumulation in estuarine and coastal sediments: The influence of H2S on dissimilatory nitrate reduction. Estuar Coast Shelf Sci 67:231–8.  https://doi.org/10.1016/j.ecss.2005.11.021.CrossRefGoogle Scholar
  80. Silver WL, Herman DJ, Firestone MK. 2001. Dissimilatory nitrate reduction to ammonium in upland tropical forest soils. Ecology 82:2410–16.CrossRefGoogle Scholar
  81. Smith JM, Ogram A. 2008. Genetic and functional variation in denitrifier populations along a short-term restoration chronosequence. Appl Environ Microbiol 74:5615–20.  https://doi.org/10.1128/AEM.00349-08.CrossRefPubMedPubMedCentralGoogle Scholar
  82. Smyth AR, Thompson SP, Siporin KN, Gardner WS, McCarthy MJ, Piehler MF. 2013. Assessing nitrogen dynamics throughout the estuarine landscape. Estuaries Coast 36:44–55.CrossRefGoogle Scholar
  83. Spalding EA, Hester MW. 2007. Interactive effects of hydrology and salinity on oligohaline plant species productivity: implications of relative sea-level rise. Estuaries Coast 30:214–25.CrossRefGoogle Scholar
  84. Tiedje JM. 1988. Ecology of denitrification and dissimilatory nitrate reduction to ammonium. In: Environmental microbiology of anaerobes. New York: Wiley. p 179–244.Google Scholar
  85. Tobias CR, Neubauer SC. 2009. Salt marsh biogeochemistry—an overview. In: Perillo GME, Wolanski E, Cahoon DR, Brinson MM, Eds. Coastal wetlands: an integrated ecological approach. Elsevier. p 445–92.Google Scholar
  86. van Diggelen JMH, Lamers LPM, van Dijk G, Schaafsma MJ, Roelofs JGM, Smolders AJP. 2014. New insights into phosphorus mobilisation from sulphur-rich sediments: time-dependent effects of salinisation. PLoS ONE 9:15–19.  https://doi.org/10.1371/journal.pone.0111106.CrossRefGoogle Scholar
  87. van Dijk G, Smolders AJP, Loeb R, Bout A, Roelofs JGM, Lamers LPM. 2015. Salinization of coastal freshwater wetlands; effects of constant versus fluctuating salinity on sediment biogeochemistry. Biogeochemistry 126:71–84.  https://doi.org/10.1007/s10533-015-0140-1.CrossRefGoogle Scholar
  88. Von Korff BH, Piehler MF, Ensign SH. 2014. Comparison of denitrification between river channels and their adjoining tidal freshwater wetlands. Wetlands 34:1047–60.  https://doi.org/10.1007/s13157-014-0545-y.CrossRefGoogle Scholar
  89. Weston NB, Dixon RE, Joye SB. 2006. Ramifications of increased salinity in tidal freshwater sediments: Geochemistry and microbial pathways of organic matter mineralization. J Geophys Res 111:G01009.  https://doi.org/10.1029/2005JG000071.CrossRefGoogle Scholar
  90. Weston NB, Giblin AE, Banta GT, Hopkinson CS, Tucker J. 2010. The effects of varying salinity on ammonium exchange in estuarine sediments of the Parker River, Massachusetts. Estuaries Coast 33:985–1003.  https://doi.org/10.1007/s12237-010-9282-5.CrossRefGoogle Scholar
  91. Weston NB, Neubauer SC, Velinsky DJ, Vile MA. 2014. Net ecosystem carbon exchange and the greenhouse gas balance of tidal marshes along an estuarine salinity gradient. Biogeochemistry 120:163–89.  https://doi.org/10.1007/s10533-014-9989-7.CrossRefGoogle Scholar
  92. Weston NB, Vile MA, Neubauer SC, Velinsky DJ. 2011. Accelerated microbial organic matter mineralization following salt-water intrusion into tidal freshwater marsh soils. Biogeochemistry 102:135–51.  https://doi.org/10.1007/s10533-010-9427-4.CrossRefGoogle Scholar
  93. Yin C, Fan F, Song A, Li Z, Yu W, Liang Y. 2014. Different denitrification potential of aquic brown soil in Northeast China under inorganic and organic fertilization accompanied by distinct changes of nirS- and nirK-denitrifying bacterial community. Eur J Soil Biol 65:47–56.  https://doi.org/10.1016/j.ejsobi.2014.09.003.CrossRefGoogle Scholar
  94. Yoshida M, Ishii S, Otsuka S, Senoo K. 2009. Temporal shifts in diversity and quantity of nirS and nirK in a rice paddy field soil. Soil Biology and Biochem 41:2044–51.  https://doi.org/10.1016/j.soilbio.2009.07.012.CrossRefGoogle Scholar
  95. Zheng Y, Hou L, Liu M, Liu Z, Li X, Lin X, Yin G, Gao J, Yu C, Wang R, Jiang X. 2016. Tidal pumping facilitates dissimilatory nitrate reduction in intertidal marshes. Sci Rep 6:1–12.  https://doi.org/10.1038/srep21338.CrossRefGoogle Scholar
  96. Zhou M, Butterbach-Bahl K, Vereecken H, Brüggemann N. 2017. A meta-analysis of soil salinization effects on nitrogen pools, cycles and fluxes in coastal ecosystems. Glob Change Biol 23:1338–52.  https://doi.org/10.1111/gcb.13430.CrossRefGoogle Scholar

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Authors and Affiliations

  • Scott C. Neubauer
    • 1
    • 2
    Email author
  • Michael F. Piehler
    • 3
  • Ashley R. Smyth
    • 3
    • 4
  • Rima B. Franklin
    • 5
  1. 1.Baruch Marine Field LaboratoryUniversity of South CarolinaGeorgetownUSA
  2. 2.Department of BiologyVirginia Commonwealth UniversityRichmondUSA
  3. 3.Institute of Marine Sciences, University of North Carolina at Chapel HillMorehead CityUSA
  4. 4.Soil and Water Sciences DepartmentTropical Research and Education Center, University of FloridaHomesteadUSA
  5. 5.Department of BiologyVirginia Commonwealth UniversityRichmondUSA

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