Nitrous oxide emission from Ulva lactuca incubated in batch cultures is stimulated by nitrite, nitrate and light

Journal of Experimental Marine Biology and Ecology

Volumn 448, Issue , 2013, Pages 37-45

  Albert, Kristian Rost ^a   Bruhn, Annette ^b   Ambus, Per ^a  

^a TECHNICAL UNIVERSITY OF DENMARK   (Denmark)

^b AARHUS UNIVERSITY   (Denmark)

Author keywords

Biomass production; GHG emission; Global warming potential; Macroalgae

Indexed keywords

ALGAL CULTURE; BIOGENIC EMISSION; BIOMASS; CARBON DIOXIDE; ENZYME ACTIVITY; FOSSIL FUEL; GLOBAL WARMING; GREEN ALGA; GREENHOUSE GAS; LIFE CYCLE ANALYSIS; LIGHT EFFECT; MACROALGA; NITRATE; NITRITE; NITROUS OXIDE; PHOTOSYNTHESIS; RENEWABLE RESOURCE;

EID: 84880392910     PISSN: 00220981     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jembe.2013.06.010     Document Type: Article

References (70)

1. Adler P.R., Del Grosso S.J., Parton W.J. Life-cycle assessment of net greenhouse-gas flux for bioenergy cropping systems. Ecol. Appl. 2007, 17:675-691.
2. Alegria A.E., Sanchez S., Quintana I. Quinone-enhanced ascorbate reduction of nitric oxide: role of quinine redox potential. Free Radic. Res. 2004, 38:1107-1112.
3. Bange H.W. Nitrous oxide and methane in European coastal waters. Estuarine Coastal Shelf Sci. 2006, 70:361-374.
4. Berges J.A. Minireview: algal nitrate reductases. Eur. J. Phycol. 1997, 32:3-8.
5. Bird M.I., Wurster C.M., Silva P.H.D., Bass A.M., de Nys R. Algal biochar - production and properties. Bioresour. Technol. 2011, 102:1886-1891.
6. Bruhn A., Dahl J., Bangsø Nielsen H., Nikolajsen L., Rasmussen M.B., Markager S., Olesen B., Carlos A., Jensen P.D. Bioenergy potential of Ulva lactuca: biomass yield, methane production and combustion. Bioresour. Technol. 2011, 102:2595-2604.
7. Cabello-Pasini A., Aguirre-von-Wobeser E., Figueroa F.L. Photoinhibition of photosynthesis in Macrocystis pyrifera (Phaeophyceae), Chondrus crispus (Rhodophyceae) and Ulva lactuca (Chlorophyceae) in outdoor culture systems. J. Photochem. Photobiol. B 2000, 57:169-178.
8. Cahill P.L., Hurd C.L., Lokman M. Keeping the water clean - seaweed biofiltration outperforms traditional bacterial biofilms in recirculating aquaculture 2010, 306:153-159.
9. Campbell W.H. Nitrate reductase structure, function and regulation: bridging the gap between biochemistry and physiology. Annu. Rev. Plant Physiol. Plant Mol. Biol. 1999, 50:277-303.
10. Chopin T., Sawhney M. Seaweeds and their mariculture. Ecological Engineering 2009, 3:4477-4486. Elsevier, Oxford, UK. S.E. Jörgensen, B.D. Fath (Eds.).
11. Chung I.K., Beardall J., Mehta S., Sahoo D., Stojkovic S. Using marine macroalgae for carbon sequestration: a critical appraisal. J. Appl. Phycol. 2011, 23:877-886.
12. Codispoti L.A., Yoshinari T., Devol A.H. Suboxic respiration in the oceanic water column. Respiration in Aquatic Ecosystems 2005, 225-247. Oxford University Press, Oxford. P.A. Del Giorgio, P.J. Williams, B. le (Eds.).
13. Dean J.V., Harper J.E. The conversion of nitrite to nitrogen oxide(s) by the constitutive NAD(P)H-nitrate reductase enzyme from soybean. Plant Physiol. 1988, 82:389-395.
14. Ducluzeau A.-L., van Lis R., Duval S., Schoepp-Cothenet B., Russel M.J., Nitschke W. Was nitric oxide the first deep electron sink?. Trends Biochem. Sci. 2009, 34:9-15.
15. Fernandez E., Galvan A. Inorganic nitrogen assimilation in Chlamydomonas. J. Exp. Bot. 2007, 58:2279-2287.
16. Forde B.G. Nitrate transporters in plants: structure, function and regulation. Biochim. Biophys. Acta Biomembr. 2000, 1465:219-235.
17. Foyer C.H., Noctor G., Hodges M. Respiration and nitrogen assimilation: targeting mitochondria-associated metabolism as a means to enhance nitrogen use efficiency. J. Exp. Bot. 2011, 62:1467-1482.
18. Galvan A., Reach J., Marisal V., Fernandez E. Nitrite transport to the chloroplast in Chlamydomonas reinhardtii: molecular evidence for a regulated process. J. Exp. Bot. 2002, 53:845-853.
19. Gao Y., Smith G.J., Alberte R.S. Light regulation of nitrate reductase in Ulva fenestrata (Chlorophyceae). Influence of light regimes on nitrate reductase activity. Mar. Ecol. 1992, 112:691-696.
20. Garcia H.E., Locarnini R.A., Boyer T.P., Antonov J.I. Volume 4: nutrients. World Ocean Atlas 2005 2006, US goverment printing office, (http://www.nodc.noaa.gov/OC5/WOA05/pubwoa05.html). S. Levitus (Ed.).
21. Glass A.D.M. Nitrogen use efficiency of crop plants: physiological constraints upon nitrogen absorption. Crit. Rev. Plant Sci. 2003, 22:453-470.
22. 2O by nitrifying bacteria at reduced concentrations of oxygen. Appl. Environ. Microbiol. 1980, 40:526-532.
23. 2O) from transgenic tobacco expressing antisense NiR mRNA. Plant J. 1999, 19:75-80.
24. Groffman P.M., Gold A.J., Addy K. Nitrous oxide production in riparian zones and its importance to national emission inventories. Chemosphere Global Chang. Sci. 2000, 2:291-299.
25. Guillard R.R.L. Culture of phytoplankton for feeding invertebrates. Culture of Marine Invertebrate Animals 1975, 26-60. Plenum Press, New York, USA. W.L. Smith, P. Chanley (Eds.).
26. Gupta K.J., Alisdair A.R., Kaiser W.M., van Dongen J.T. On the origin of nitric oxide. Trends Plant Sci. 2010, 16:160-168.
27. Gupta K.J., Igamberdiev A.U., Manjunatha G., Segu S., Moran J.F., Neelawarne B., Bauwe H., Kaiser W.M. The emerging roles of nitric oxide (NO) in plant mitochondria. Plant Sci. 2011, 181:520-526.
28. Hakata M., Takahasi M., Zumft W., Sakamoto A., Morikawa H. Conversion of nitrate nitrogen and nitrogen dioxide to nitrous oxides in plants. Acta Biotechnol. 2003, 23:249-257.
29. Hanelt D. Photoinhibition of photosynthesis in marine macroalgae. Sci. Mar. 1996, 60:243-248.
30. Hein M., Pedersen M.F., Sand-Jensen K. Size-dependent nitrogen uptake in micro- and macroalgae. Mar. Ecol. Prog. Ser. 1995, 118:247-253.
31. Igamberdiev A.U., Hill R.D. Plant mitochondrial function during anaerobiosis. Ann Bot 2009, 103:259-268.
32. Igamberdiev A.U., Bykova N.V., Shah J.K., Hill R.D. Anoxic nitric oxide cycling in plants, participating reactions and possible mechanisms. Physiol. Plant. 2010, 138:393-404.
33. 2O budget: a retrospective analysis 1500-1994. Global Biogeochem. Cycles 1999, 13:1-8.
34. Lahaye M., Robic A. Structure and functional properties of Ulvan, a polysaccharide from green seaweeds. Biomacromlecules 2007, 8:1764-1774.
35. Lam P., Kuypers M.M.M. Microbial nitrogen cycling processes in oxygen minimum zones. Annual Review of Marine Science 2011, 3:317-345. C.A. Carlson, S.J. Giovannoni (Eds.).
36. Law C.S., Rees A.P., Owens N.J.P. Nitrous oxide production by estuarine epiphyton. Limnol. Oceanogr. 1993, 38:435-441.
37. Lewis L.A., McCourt R.M. Green algae and the origin of land plants. Am. J. Bot. 2004, 91:1535-1556.
38. Littler M.M., Littler D.S. The evolution of thallus form and survival strategies in benthic marine macroalgae: field and laboratory tests of a functional form model. Am. Nat. 1980, 116:25-44.
39. Longstaff B.J., Kildea T., Runcie J.W., Cheshire A., Dennison W.C., Hurd C., Kana T., Raven J.A., Larkum A.W.D. An in situ study of photosynthetic oxygen exchange and electron transport rate in the marine macroalga Ulva lactuca (Chlorophyta). Photosynth. Res. 2002, 74:281-293.
40. Mallick N., Mohn F.H., Doeder C.J. Evidence supporting nitrite dependent NO release by green microalga Scenedesmus obliquus. J. Plant Physiol. 2000, 157:40-46.
41. McHugh D.J. A guide to the seaweed industry. FAO Fisheries Technical Paper No. 441 2003, FAO, Rome, Italy, (118 pp.).
42. Msuya F.E., Neori A. Effect of water aeration and nutrient level on biomass yield, N uptake and protein content of the seaweed Ulva lactuca cultured in seawater tanks. J. Appl. Phycol. 2008, 20:1021-1031.
43. Nielsen M.M., Bruhn A., Rasmussen M.B., Olesen B., Larsen M.M., Møller H.B. Cultivation of Ulva lactuca with manure for simultaneous bioremediation and biomass production. J. Appl. Phycol. 2012, 24:449-458.
44. Pedersen M.F. Nitrogen limitation of photosynthesis and growth: comparison across aquatic plant communities in a Danish estuary (Roskilde Fjord). Ophelia 1995, 41:61-272.
45. Pedersen M.F., Borum J. Nutrient control of algal growth in estuarine waters: nutrient limitation and the importance of nitrogen requirements and nitrogen storage among phytoplankton and species of macroalgae. Mar. Ecol. Prog. Ser. 1996, 142:261-272.
46. Prather M., Ehhalt D. Atmospheric chemistry and greenhouse gases. Climate Change 2001: The Scientific Basis 2001, 239-287. Cambridge University Press, Cambridge, UK, (Chapter 4). J.T. Houghton (Ed.).
47. Rai L.C., Kumar H.D., Mohn F.H., Soeder C.J. Services of algae to the environment. J. Microbiol. Biotechnol. 2000, 10:119-136.
48. Rees T.A.V. Safety factors and nutrient uptake by seaweeds. Mar. Ecol. Prog. Ser. 2003, 263:29-42.
49. Rees T.A.V., Dobson B.C., Bijl M., Morelissen B. Kinetics of nitrate uptake by New Zealand marine macroalgae and evidence for two nitrate transporters in Ulva intestinalis L. Hydrobiologia 2007, 586:135-141.
50. Rivers J.S., Peckol P. Summer decline of Ulva lactuca (Chlorophyta) in a eutrophic embayment: interactive effects of temperature and nitrogen availability. J. Phycol. 1995, 312:223-228.
51. Rosenberg G., Ramus J. Uptake of inorganic nitrogen and seaweed surface area: volume ratios. Aquat. Bot. 1984, 19:65-72.
52. Runcie J.W., Ritchie R.J., Larkum A.W. Uptake kinetics and assimilation of inorganic nitrogen by Catenella nipae and Ulva lactuca. Aquat. Bot. 2003, 76:155-174.
53. Ryther J.H., Debusk T.A., Blakeslee M. Cultivation and conversion of marine macroalgae. (Gracilaria and Ulva). SERI/STR-231-2360 1984, 1-88.
54. Sakihama Y., Nakamura S., Yamasaki H. Nitric oxide production by nitrate reductase in green alga Chlamydomonas reinhardtii: an alternative NO production pathway in photosynthetic organisms. Plant Cell Physiol. 2002, 43:290-297.
55. 2O emissions from aquatic systems: natural emissions and anthropogenic effects. Chemosphere Global Chang. Sci. 2000, 2:267-279.
56. Smart D.R., Bloom A.J. Wheat leaves emit nitrous oxide during nitrate assimilation. Proc. Natl. Acad. Sci. U. S. A. 2001, 98:7875-7878.
57. Solomonson L.P., Barber M.J. Assimilatory nitrate reductase: functional properties and regulation. Annu. Rev. Plant Physiol. Plant Mol. Biol. 1990, 41:225-253.
58. Stief P., Poulsen M., Nielsen L.P., Brix H., Schramm A. Nitrous oxide emission by aquatic macrofauna. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:4296-4300.
59. Taylor G. Biofuels and the biorefinery concept. Energy Policy 2008, 36:4406-4409.
60. -3 transporter?. Plant Physiol. 1997, 114:137-144.
61. UNEP United Nations Environment Programme. Global Environment Outlook Year Book 2003 2004, UNEP, Nairobi, Kenya, (76 pp.).
62. Wang H.J., Wang W.D., Yin C.Q., Wang Y.C., Lu J.W. Littoral zones as the "hotspots" of nitrous oxide (N2O) emission in a hyper-eutrophic lake in China. Atmos. Environ. 2006, 40:5522-5527.
63. 2O) fluxes and their relationships with water-sediment characteristics in a hyper-eutrophic shallow lake, China. J. Geophys. Res. 2007, 112:G01005. 10.1029/2005JG000129.
64. 2O evolution by green algae. Appl. Environ. Microbiol. 1984, 48:1251-1253.
65. Weathers P.J., Niedzielski J.J. Nitrous oxide production by cyanobacteria. Arch. Microbiol. 1986, 146:204-206.
66. 2O emission from soil under different moisture regimes. Biol. Fertil. Soils 1996, 22:331-335.
67. Weis R.F., Price B.A. Nitrous oxide solubility in water and seawater. Mar. Chem. 1980, 8:347-359.
68. Wilson I., Neill S.J., Hancock J.T. Nitric oxide synthesis and signaling in plants. Plant Cell Environ. 2008, 31:622-631.
69. Wrage N., Velthof G.L., van Beusichem M.L., Oenema O. Role of nitrifier denitrification in the production of nitrous oxide. Soil Biol. Biochem. 2001, 33:1723-1732.
70. Yamasaki H., Shimoji H., Ohshiro Y., Sakihama Y. Inhibitory effects of nitric oxide on oxidative phosphorylation in plant mitochondria. Nitric Oxide Biol. Chem. 2001, 5:261-270.