Denitrification by benthic foraminifera and their contribution to N-loss from a fjord environment

Abstract. Oxygen and nitrate availabilities impact the marine nitrogen cycle at a range of spatial and temporal scales. Here, we demonstrate the impact of denitrifying foraminifera on the nitrogen cycle at two oxygen and nitrate contrasting stations in a fjord environment (Gullmar Fjord, Sweden). Denitrification by benthic foraminifera was determined through the combination of specific density counting per microhabitat and specific nitrate respiration rates obtained through incubation experiments using N2O microsensors. Benthic nitrate removal was calculated from submillimeter chemical gradients extracted from 2D porewater images of the porewater nitrate concentration. These were acquired by combining the DET technique (diffusive equilibrium in thin film) with chemical colorimetry and hyperspectral imagery. Sediments with high nitrate concentrations in the porewater and oxygenated overlying water were dominated by the non-indigenous species (NIS) Nonionella sp. T1. Denitrification by this species could account for 50 %–100 % of the nitrate loss estimated from the nitrate gradients. In contrast sediments below hypoxic bottom waters had low inventories of porewater nitrate, and denitrifying foraminifera were rare. Their contribution to benthic nitrate removal was negligible (  5 %). Our study showed that benthic foraminifera can be a major contributor to nitrogen mitigation in oxic coastal ecosystems and should be included in ecological and diagenetic models aiming to understand biogeochemical cycles coupled to nitrogen.

[1]  J. Spangenberg,et al.  Surviving anoxia in marine sediments: The metabolic response of ubiquitous benthic foraminifera (Ammonia tepida) , 2017, PloS one.

[2]  P. Stief.  Stimulation of microbial nitrogen cycling in aquatic ecosystems by benthic macrofauna: mechanisms and environmental implications , 2013 .

[3]  S. Hietanen,et al.  The Effects of Hypoxia on Sediment Nitrogen Cycling in the Baltic Sea , 2012, AMBIO.

[4]  Kjell Nordberg,et al.  Decreasing oxygen concentrations in the Gullmar Fjord, Sweden, as confirmed by benthic foraminifera, and the possible association with NAO , 2000 .

[5]  Kjell Nordberg,et al.  Climate variations, an overlooked factor influencing the recent marine environment. An example from Gullmar Fjord, Sweden, illustrated by benthic foraminifera and hydrographic data , 2004 .

[6]  R. Herbert.  Nitrogen cycling in coastal marine ecosystems. , 1999, FEMS microbiology reviews.

[7]  D. Jézéquel,et al.  Simultaneous Nitrite/Nitrate Imagery at Millimeter Scale through the Water-Sediment Interface. , 2016, Environmental science & technology.

[8]  P. Hall,et al.  Biogeochemical heterogeneity and suboxic diagenesis in hemipelagic sediments of the Panama Basin , 1998 .

[9]  M. Stachowitsch.  Mass Mortality in the Gulf of Trieste: The Course of Community Destruction , 1984 .

[10]  D. Gilbert,et al.  Natural and human-induced hypoxia and consequences for coastal areas: synthesis and future development , 2009 .

[11]  Lars Peter Nielsen,et al.  Evidence for complete denitrification in a benthic foraminifer , 2006, Nature.

[12]  S. Sommer,et al.  Biological nitrate transport in sediments on the Peruvian margin mitigates benthic sulfide emissions and drives pelagic N loss during stagnation events , 2016 .

[13]  Kjell Nordberg,et al.  Foraminiferal fauna from a deep basin in Gullmar Fjord: The influence of seasonal hypoxia and North Atlantic Oscillation , 2013 .

[14]  Denis Gilbert,et al.  Dynamics and distribution of natural and human-caused hypoxia , 2010 .

[15]  D. Kirchman.  Microbial ecology of the oceans , 2008 .

[16]  D. Jézéquel,et al.  Simultaneous 2D imaging of dissolved iron and reactive phosphorus in sediment porewaters by thin-film and hyperspectral methods. , 2014, Environmental science & technology.

[17]  D. Sigman,et al.  Nitrogen Isotopes in the Ocean , 2019 .

[18]  Michael R. Roman,et al.  Eutrophication of Chesapeake Bay: historical trends and ecological interactions , 2005 .

[19]  W. Kemp,et al.  Denitrification in coastal ecosystems: methods, environmental controls, and ecosystem level controls, a review , 1999, Aquatic Ecology.

[20]  R. Díaz.  Overview of hypoxia around the world. , 2001, Journal of environmental quality.

[21]  I. Davies,et al.  Anoxic nitrification in marine sediments , 2004 .

[22]  N. Risgaard-Petersen,et al.  Vertical migration, nitrate uptake and denitrification: survival mechanisms of foraminifers (Globobulimina turgida) under low oxygen conditions. , 2011, FEMS microbiology ecology.

[23]  R. Aller,et al.  The Effects of Macrobenthos on Chemical Properties of Marine Sediment and Overlying Water , 1982 .

[24]  G. Asner,et al.  Nitrogen Cycles: Past, Present, and Future , 2004 .

[25]  L. Hernroth,et al.  Phyto-Zooplankton Community in Coastal Waters of Western Sweden -An Ecosystem Off Balance? , 1983 .

[26]  B. Thamdrup,et al.  Controls on Mo isotope fractionations in a Mn-rich anoxic marine sediment, Gullmar Fjord, Sweden , 2012 .

[27]  H. Nomaki,et al.  Variation in the nitrogen isotopic composition of amino acids in benthic foraminifera: Implications for their adaptation to oxygen‐depleted environments , 2015 .

[28]  C. Deutsch,et al.  New developments in the marine nitrogen cycle. , 2007, Chemical reviews.

[29]  Rapid environmental responses to climate-induced hydrographic changes in the Baltic Sea entrance , 2019, Biogeosciences.

[30]  A. Townsend‐Small,et al.  Denitrification in anoxic sediments supported by biological nitrate transport , 2011 .

[31]  R. Xiang,et al.  Live benthic foraminifera in the Yellow Sea and the East China Sea: vertical distribution, nitrate storage, and potential denitrification , 2017 .

[32]  P. Rosenstiel,et al.  A novel eukaryotic denitrification pathway in foraminifera , 2018, Current Biology.

[33]  R. Rosenberg,et al.  Spreading Dead Zones and Consequences for Marine Ecosystems , 2008, Science.

[34]  L. Arneborg.  Turnover times for the water above sill level in Gullmar Fjord , 2004 .

[35]  J. Schönfeld,et al.  Recent invasion of the foraminifer Nonionella stella Cushman & Moyer, 1930 in northern European waters: evidence from the Skagerrak and its fjords , 2015 .

[36]  J. Duchêne,et al.  How does macrofaunal bioturbation influence the vertical distribution of living benthic foraminifera , 2016 .

[37]  F. Jorissen,et al.  Oxygen respiration rates of benthic foraminifera as measured with oxygen microsensors , 2011 .

[38]  J. Laybourn-Parry,et al.  Respiration rates and biovolumes of common benthic Foraminifera (Protozoa) , 1994, Journal of the Marine Biological Association of the United Kingdom.

[39]  F. Jorissen,et al.  Widespread occurrence of nitrate storage and denitrification among Foraminifera and Gromiida , 2009, Proceedings of the National Academy of Sciences.

[40]  Kjell Nordberg,et al.  LIVING (STAINED) BENTHIC FORAMINIFERAL RESPONSE TO PRIMARY PRODUCTION AND HYDROGRAPHY IN THE DEEPEST PART OF THE GULLMAR FJORD, SWEDISH WEST COAST, WITH COMPARISONS TO HÖGLUND’S 1927 MATERIAL , 2001 .

[41]  M. Chierici,et al.  The effects of multiple stressors on the distribution of coastal benthic foraminifera: A case study from the Skagerrak-Baltic Sea region , 2018 .

[42]  N. Risgaard-Petersen,et al.  Nitrate Storage and Dissimilatory Nitrate Reduction by Eukaryotic Microbes , 2015, Front. Microbiol..

[43]  L. Nielsen,et al.  Denitrification, nitrate turnover, and aerobic respiration by benthic foraminiferans in the oxygen minimum zone off Chile , 2008 .

[44]  S. Seitzinger.  Denitrification in freshwater and coastal marine ecosystems: Ecological and geochemical significance , 1988 .

[45]  L. Proctor,et al.  Sediment denitrification in the Gulf of Mexico zone of hypoxia , 2002 .

[46]  A. Devol.  Denitrification Including Anammox , 2008 .

[47]  S. Goldstein,et al.  � 2003, by the American Society of Limnology and Oceanography, Inc. Propagule transport as a key method of dispersal in benthic foraminifera (Protista) , 2022 .

[48]  Kjell Nordberg,et al.  Upwelling along the Swedish west coast during the 20th century , 2003 .

[49]  A. Belgrano,et al.  Primary production, climatic oscillations, and physico-chemical processes: the Gullmar Fjord time-series data set (1985–1996) , 1998 .

[50]  B. Seibel,et al.  Declining oxygen in the global ocean and coastal waters , 2018, Science.

[51]  R. Aller,et al.  The sedimentary Mn cycle in Long Island Sound: Its role as intermediate oxidant and the influence of bioturbation, O 2 , and C org flux on diagenetic reaction balances , 1994 .

[52]  Peter Berg,et al.  Interpretation of measured concentration profiles in sediment pore water , 1998 .

[53]  M. McIlvin,et al.  Denitrification likely catalyzed by endobionts in an allogromiid foraminifer , 2011, The ISME Journal.

[54]  N. Risgaard-Petersen,et al.  Oxygen regulation of nitrification and denitrification in sediments , 1994 .

[55]  P. Viaroli,et al.  Implications for oxygen, nutrient fluxes and denitrification rates during the early stage of sediment colonisation by the polychaete Nereis spp. in four estuaries , 2007 .

[56]  W. Boynton,et al.  Ammonium recycling versus denitrification in chesapeake bay sediments , 1990 .

[57]  Hao Zhang,et al.  Micro-scale biogeochemical heterogeneity in sediments : a review of available technology and observed evidence. , 2009 .

[58]  J. Carstensen,et al.  Spatial and temporal resolution of carbon fluxes in a shallow coastal ecosystem, the Kattegat , 2003 .

[59]  L. Levin,et al.  Effects of natural and human-induced hypoxia on coastal benthos , 2009 .

[60]  S. Hulth,et al.  Coupled anoxic nitrification/manganese reduction in marine sediments , 1999 .

[61]  N. Revsbech,et al.  An oxygen microsensor with a guard cathode , 1989 .

[62]  V. Bouchet,et al.  History of the introduction of a species resembling the benthic foraminifera Nonionella stella in the Oslofjord (Norway): morphological, molecular and paleo-ecological evidences , 2019, Aquatic Invasions.

[63]  A. Svansson.  Physical and chemical oceanography of the Skagerrak and the Kattegat. , 1975 .

[64]  P. Hallock,et al.  DORMANCY IN THE FORAMINIFERA: A REVIEW , 2016 .

[65]  Nicolas Gruber,et al.  Global patterns of marine nitrogen fixation and denitrification , 1997 .

[66]  Denis Gilbert,et al.  Dynamics and distribution of natural and human-caused coastal hypoxia , 2009 .

[67]  R. Rosenberg,et al.  The Impact of Benthic Macrofauna for Nutrient Fluxes from Baltic Sea Sediments , 2007, Ambio.

[68]  J. Bernhard,et al.  Comparison of two methods to identify live benthic foraminifera: A test between Rose Bengal and CellTracker Green with implications for stable isotope paleoreconstructions , 2006 .

[69]  P. Christensen,et al.  Sediment mineralization, nutrient fluxes, denitrification and dissimilatory nitrate reduction to ammonium in an estuarine fjord with sea cage trout farms , 2000 .

[70]  N. Revsbech,et al.  An oxygen insensitive microsensor for nitrous oxide , 2001 .

[71]  Jacob Carstensen,et al.  LONG-TERM CHANGES AND IMPACTS OF HYPOXIA IN DANISH COASTAL WATERS , 2007 .

[72]  P. Engström,et al.  Anaerobic ammonium oxidation by nitrite (anammox): Implications for N2 production in coastal marine sediments , 2005 .

[73]  Bjørn Sundby,et al.  Interactions of manganese with the nitrogen cycle: Alternative pathways to dinitrogen , 1997 .

[74]  S. Sommer,et al.  The role of benthic foraminifera in the benthic nitrogen cycle of the Peruvian oxygen minimum zone , 2012 .

[75]  M. Trimmer,et al.  The potential effect of sustained hypoxia on nitrogen cycling in sediment from the southern North Sea: a mesocosm experiment , 2013, Biogeochemistry.

[76]  Kjell Nordberg.  Oceanography in the Kattegat and Skagerrak Over the Past 8000 Years , 1991 .

[77]  S. Bowser,et al.  Sinks and Sources of Intracellular Nitrate in Gromiids , 2017, Front. Microbiol..

[78]  Kjell Nordberg,et al.  Tracing winter temperatures over the last two millennia using a north-east Atlantic coastal record , 2018, Climate of the Past.

[79]  S. Sommer,et al.  Metabolic preference of nitrate over oxygen as an electron acceptor in foraminifera from the Peruvian oxygen minimum zone , 2019, Proceedings of the National Academy of Sciences.