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Vegetation loss decreases salt marsh denitrification capacity: Implications for marsh erosion Sarra E. Hinshaw, Corianne Tatariw, Nikaela Flournoy, Alice Kleinhuizen, Caitlin Bailey Taylor, Patricia Sobecky, and Behzad Mortazavi Environ. Sci. Technol., Just Accepted Manuscript • DOI: 10.1021/acs.est.7b00618 • Publication Date (Web): 15 Jun 2017 Downloaded from http://pubs.acs.org on June 19, 2017
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Title: Vegetation loss decreases salt marsh denitrification capacity: Implications for marsh erosion Authors: Sarra E. Hinshaw1 2*, Corianne Tatariw1 2*, Nikaela Flournoy1, Alice Kleinhuizen1 2, Caitlin Taylor1, Patricia Sobecky1, Behzad Mortazavi1 2** Authors address: 1University of Alabama, Department of Biological Sciences, Tuscaloosa, AL 35487, 2Dauphin Island Sea Lab, Dauphin Island, AL 36528 *S.E.H. and C.T. have contributed equally to this manuscript **Corresponding Author University of Alabama Dauphin Island Sea Laboratory 101 Bienville Blvd Dauphin Island, AL 36528 251-861-2141
[email protected] Keywords: Deepwater Horizon, isotope pairing, Chandeleur Islands, Spartina alterniflora, napA, nirS, norB, nutrient flux
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ABSTRACT
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Salt marshes play a key role in removing excess anthropogenic nitrogen (N)
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loads to nearshore marine ecosystems through sediment microbial processes such as
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denitrification. However, in the Gulf of Mexico the loss of marsh vegetation due to
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human-driven disturbances such as sea level rise and oil spills can potentially reduce
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marsh capacity for N removal. In order to investigate the effect of vegetation loss on
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ecosystem N removal, we contrasted denitrification capacity in marsh and subtidal
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sediments impacted by the Deepwater Horizon oil spill using a combination of 29N2 and
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block), and quantitative PCR (qPCR) of functional genes in the denitrification pathway.
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We found that, on average, denitrification capacity was four times higher in vegetated
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sediments due to a combination of enhanced nitrification and higher organic carbon
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availability. The abundance of nirS-type denitrifers indicated that marsh vegetation
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regulates the activity, rather than the abundance, of denitrifier communities. We
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estimated that marsh sediments remove an average of 3.6 t N km-2y-1 compared to 0.9 t
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N km-2y-1 in unvegetated sediments. Overall, our findings indicate that marsh loss
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results in a substantial loss of N removal capacity in coastal ecosystems.
N2 production (isotope pairing), denitrification potential measurements (acetylene
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1. INTRODUCTION
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Human activity has more than doubled the amount of biologically available
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nitrogen (N) in the environment1, resulting in negative environmental impacts in coastal
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ecosystems, such as harmful algal blooms (HABs) and hypoxia2,3. By removing up to
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33% of reactive N they receive worldwide4, salt marshes mitigate N loads to coastal
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ecosystems, providing a highly valuable ecosystem service5,6. However, marshes in
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Europe, North America, Australia and China declined by as much as 50% during the
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20th century7,8. This worldwide trend is reflected in the United States along the Louisiana
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(USA) coast in the northern Gulf of Mexico (nGoM), where a combination of reduced
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sediment loads associated with land use change, sea level rise, and subsidence
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contributed to the loss of 23% Louisiana’s marshes since the 1930s9,10. Furthermore,
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marshes appear increasingly susceptible to disturbances such as changing precipitation
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patterns11, eutrophication12, and oil spills13.
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Denitrification is a microbially-mediated process by which nitrate (NO3-) is
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reduced through a series of stepwise reactions to nitric oxide (NO), nitrous oxide (N2O)
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and dinitrogen (N2) gases14,15. Denitrification occurs in most coastal habitats, but salt
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marshes in particular provide favorable conditions for increased N removal via
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denitrification16 in part due to their vegetation6,17. Salt marsh vegetation promotes
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denitrification by providing organic carbon via labile root exudates and organic matter18–
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nitrification-denitrification at the oxic/anoxic interface21,22. Therefore, when marsh
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vegetation is lost, there is a subsequent loss of sediment denitrification capacity.
. Rhizosphere oxygen (O2) transport into the sediment anoxic zone promotes coupled
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Although the link between salt marsh collapse and reduced biogeochemical
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function is well established23,24, less is known about how much of marsh response to
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disturbance is mediated through changes in the functional microbial community. Both
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changes in tidal flow and marsh fertilization have been shown to alter denitrifier
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abundance and diversity in salt marshes25,26, but changes in denitrifier community
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composition and gene expression do not necessarily correspond to changes in
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denitrification rates27,28. Kearns et al.29 found that fertilization did not affect total salt
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marsh microbial community structure, but instead increased the proportion of dormant
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cells in the microbial community. However, these studies did not assess a microbial
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response to acute changes in ecosystem structure, such as salt marsh collapse
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following oil spills. The objectives of our study were to quantify the loss of function
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caused by loss of salt marsh vegetation and to determine whether environmental
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conditions or denitrifier abundance regulate denitrification in marsh sediments.
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We contrasted denitrification rates and denitrifier functional gene abundance in
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vegetated and unvegetated sediments within a few meters of the marsh’s edge (an
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environment that is similar to one when the marsh edge erodes) in the Chandeleur
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Islands; a chain of barrier islands off the coast of Louisiana subjected to moderate
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levels of oiling (based on oil band width and thickness as documented by the Shoreline
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Cleanup Assessment Technique30) during the Deepwater Horizon (DWH) oil spill. We
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hypothesized that denitrification rates would be higher in vegetated sediments due to
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increased NO3- via nitrification and labile carbon (C ) availability from rhizosphere
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processes17. We predicted that denitrifier abundance would be lower in unvegetated
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sediments, with vegetation-regulated functional community composition, rather than
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environmental conditions, being the key factor driving denitrification rates. In contrast,
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we predicted that on the marsh platform, denitrifiers would be highly abundant and
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denitrification rates would be limited by resource availability rather than genetic
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potential.
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2. MATERIAL AND METHODS
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2.1 Site Description
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Our field sites were located in the Chandeleur Islands, a chain of low-lying (
