Oxic microshield and local pH enhancement protects Zostera muelleri from sediment derived hydrogen sulphide

New Phytologist

Volumn 205, Issue 3, 2015, Pages 1264-1276

  Brodersen, Kasper Elgetti ^a   Nielsen, Daniel Aagren ^a   Ralph, Peter J ^a   Kühl, Michael ^a,b,c  

^a UNIVERSITY OF TECHNOLOGY SYDNEY   (Australia)

^b UNIVERSITY OF COPENHAGEN   (Denmark)

^c NANYANG TECHNOLOGICAL UNIVERSITY   (Singapore)

Author keywords

Biogeochemistry; Microelectrodes; Oxic microshield; Plant sediment interactions; Radial oxygen release; Rhizosphere; Zostera muelleri

Indexed keywords

ANOXIC CONDITIONS; ELECTROCHEMICAL METHOD; ENVIRONMENTAL CONDITIONS; GEOCHEMISTRY; HYDROGEN SULFIDE; PH; PHOTOSYNTHESIS; RHIZOME; SEAGRASS; SPECIATION (CHEMISTRY);

ZOSTERA MUELLERI;

HYDROGEN SULFIDE; OXYGEN; PHOTOSYSTEM II;

BIOLOGICAL MODEL; CHEMISTRY; DRUG EFFECTS; METABOLISM; PH; PHOTOSYSTEM II; QUANTUM THEORY; RHIZOME; RHIZOSPHERE; SEDIMENT; SHOOT; SPECTROFLUOROMETRY; ZOSTERACEAE;

GEOLOGIC SEDIMENTS; HYDROGEN SULFIDE; HYDROGEN-ION CONCENTRATION; MODELS, BIOLOGICAL; OXYGEN; PHOTOSYSTEM II PROTEIN COMPLEX; PLANT SHOOTS; QUANTUM THEORY; RHIZOME; RHIZOSPHERE; SPECTROMETRY, FLUORESCENCE; ZOSTERACEAE;

EID: 84920972497     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/nph.13124     Document Type: Article

References (53)

1. Almgren T, Hagstrom I. 1974. The oxidation rate of sulphide in sea water. Water Research 8: 395-400.
2. Armstrong J, Armstrong W. 2001. Rice and Phragmites: effects of organic acids on growth, root permeability, and radial oxygen loss to the rhizosphere. American Journal of Botany 88: 1359-1370.
3. Armstrong W. 1979. Aeration in higher plants. London, UK: Academic Press.
4. Barnabes AD. 1996. Casparian band-like structures in the root hypodermis of some aquatic angiosperms. Aquatic Botany 55: 217-225.
5. Beer S, Vilenkin B, Weil A, Veste M, Susel L, Eshel A. 1998. Measuring photosynthetic rates in seagrasses by pulse amplitude modulated (PAM) fluorometry. Marine Ecology Progress Series 174: 293-300.
6. Binzer T, Borum J, Pedersen O. 2005. Flow velocity affects internal oxygen conditions in the seagrass Cymodocea nodosa. Aquatic Botany 83: 239-247.
7. Borum J, Pedersen O, Greve TM, Frankovich TA, Zieman JC, Fourqurean JW, Madden CJ. 2005. The potential role of plant oxygen and sulphide dynamics in die-off events of the tropical seagrass, Thalassia testudinum. Journal of Ecology 93: 148-158.
8. Borum J, Sand-Jensen K, Binzer T, Pedersen O, Greve T. 2006. Oxygen movement in seagrasses. In: Larkum AWD, Orth JR, Duarte CM, eds. Seagrasses: biology, ecology and conservation. Dordrecht, the Netherlands: Springer, 255-270.
9. Brodersen KE, Nielsen DA, Ralph PJ, Kühl M. 2014. A split flow chamber with artificial sediment to examine the below-ground microenvironment of aquatic macrophytes. Marine Biology. doi: 10.1007/s00227-014-2542-3.
10. Caffrey JM, Kemp WM. 1991. Seasonal and spatial patterns of oxygen production, respiration and root-rhizome release in Potamogeton perfoliatus L. and Zostera marina L. Aquatic Botany 40: 109-128.
11. Carlson J, Paul R, Yarbro LA, Barber TR. 1994. Relationship of sediment sulfide to mortality of Thalassia testudinum in Florida Bay. Bulletin of Marine Science 54: 733-746.
12. 2. Environmental Science and Technology 6: 529-537.
13. Cline JD, Richards RA. 1969. Oxygenation of hydrogen sulfide in seawater at constant salinity, temperature, and pH. Environmental Science and Technology 3: 838-843.
14. Colmer TD, Gibberd MR, Wiengweera A, Thin TK. 1998. The barrier to radial oxygen loss from roots of rice (Oryza sativa L.) is induced by growth in stagnant solution. Journal of Experimental Botany 49: 1431-1436.
15. Costanza R. 1997. The value of the world's ecosystem services and natural capital. Nature 387: 253-260.
16. 2S cytotoxicity mechanism involves reactive oxygen species formation and mitochondrial depolarisation. Toxicology 203: 69-76.
17. Enstone DE, Peterson CA, Ma F. 2003. Root endodermis and exodermis: structure, function, and responses to the environment. Journal of Plant Growth Regulation 21: 335-351.
18. Fourqurean JW, Zieman JC. 2002. Nutrient content of the seagrass Thalassia testudinum reveals regional patterns of relative availability of nitrogen and phosphorus in the Florida Keys, USA. Biogeochemistry 61: 229-245.
19. Frederiksen MS, Glud RN. 2006. Oxygen dynamics in the rhizosphere of Zostera marina: a two-dimensional planar optode study. Limnology and Oceanography 51: 1072-1083.
20. Frederiksen MS, Holmer M, Borum J, Kennedy H. 2006. Temporal and spatial variation of sulfide invasion in eelgrass (Zostera marina) as reflected by its sulfur isotopic composition. Limnology and Oceanography 51: 2308-2318.
21. Goodman JL, Moore KA, Dennison WC. 1995. Photosynthetic responses of eelgrass (Zostera marina L.) to light and sediment sulfide in a shallow barrier island lagoon. Aquatic Botany 50: 37-47.
22. Greve TM, Borum J, Pedersen O. 2003. Meristematic oxygen variability in eelgrass (Zostera marina). Limnology and Oceanography 48: 210-216.
23. Holmer M, Bondgaard EJ. 2001. Photosynthetic and growth response of eelgrass to low oxygen and high sulfide concentrations during hypoxic events. Aquatic Botany 70: 29-38.
24. Holmer M, Pedersen O, Ikejima K. 2006. Sulfur cycling and sulfide intrusion in mixed Southeast Asian tropical seagrass meadows. Botanica Marina 49: 91-102.
25. Holmer M, Pedersen O, Krause-Jensen D, Olesen B, Hedegård Petersen M, Schopmeyer S, Koch M, Lomstein BA, Jensen HS. 2009. Sulfide intrusion in the tropical seagrasses Thalassia testudinum and Syringodium filiforme. Estuarine, Coastal and Shelf Science 85: 319-326.
26. Jensen SI, Kühl M, Glud RN, Jørgensen LB, Prieme A. 2005. Oxic microzones and radial oxygen loss from roots of Zostera marina. Marine Ecology Progress Series 293: 49-58.
27. Jensen SI, Kühl M, Prieme A. 2007. Different bacterial communities in the rhizoplane and bulk sediment of the seagrass Zostera marina. FEMS Microbiology Ecology 62: 108-117.
28. 2S in aquatic environments. Analytical Chemistry 68: 4351-4357.
29. 2S microgradients. Applied and Environmental Microbiology 45: 1261-1270.
30. Kühl M, Revsbech NP. 2001. Biogeochemical microsensors for boundary layer studies. In: Boudreau BP, Jørgensen BB, eds. The benthic boundary layer. New York, NY, USA: Oxford University Press, 180-210.
31. 2S microsensor for profiling sediments and biofilms: application in acidic sediment. Aquatic Microbial Ecology 15: 201-209.
32. Larkum AWD, Orth RJ, Duarte CM. 2006. Seagrasses: biology, ecology and conservation. Berlin, Germany: Springer.
33. Nelson DC, Jørgensen BB, Revsbech NP. 1986. Growth pattern and yield of a chemoautotrophic Beggiatoa sp. in oxygen-sulfide microgradients. Applied and Environmental Microbiology 52: 225-233.
34. Orth RJ, Carruthers TJB, Dennison WC, Duarte CM, Fourqurean JW, Heck KL Jr, Hughes AR, Kendrick GA, Kenworthy WJ, Olyarnik S et al. 2006. A global crisis for seagrass ecosystems. BioScience 56: 987-996.
35. Pedersen O, Binzer T, Borum J. 2004. Sulphide intrusion in eelgrass (Zostera marina L). Plant, Cell & Environment 27: 595-602.
36. Pedersen O, Borum J, Duarte CM, Fortes MD. 1998. Oxygen dynamics in the rhizosphere of Cymodocea rotundata. Marine Ecology Progress Series 169: 283-288.
37. Pedersen O, Borum J, Duarte CM, Fortes MD. 1999. ERRATUM: oxygen dynamics in the rhizosphere of Cymodocea rotundata. Marine Ecology Progress Series 178: 310.
38. Perez-Perez ME, Lemaire SD, Crespo JL. 2012. Reactive oxygen species and autophagy in plants and algae. Plant Physiology 160: 156-164.
39. Plus M, Deslous-Paoli J-M, Dagault F. 2003. Seagrass (Zostera marina L.) bed recolonisation after anoxia-induced full mortality. Aquatic Botany 77: 121-134.
40. Ralph PJ, Short FT. 2002. Impact of the wasting disease pathogen, Labyrinthula zosterae, on photobiology of eelgrass Zostera marina. Marine Ecology Progress Series 226: 265-271.
41. Ralph PJ, Tomasko D, Moore K, Seddon S, Macinnis-Ng CMO. 2006. Human impacts on seagrasses: eutrophication, sedimentation and contamination. In: Larkum AWD, Orth RJ, Duarte CM, eds. Seagrasses: biology, ecology and conservation. Berlin, Germany: Springer, 567-593.
42. Ramsing NB, Gundersen JK. 2014. Seawater and gasses: tabulated physical parameters of interest to people working with microsensors in marine systems: unisense data tables. Available from Unisense A/S, Denmark. [WWW document] URL http://www.unisense.com/files/PDF/Diverse/Seawater&Gasestable.pdf [accessed 17 September 2014].
43. Raun AL, Borum J. 2013. Combined impact of water column oxygen and temperature on internal oxygen status and growth of Zostera marina seedlings and adult shoots. Journal of Experimental Marine Biology and Ecology 441: 16-22.
44. Raven JA, Scrimgeour CM. 1997. The influence of anoxia on plants of saline habitates with special reference to the sulfur cycle. Annals of Botany 79: 79-86.
45. Revsbech NP. 1989. An oxygen microsensor with a guard cathode. Limnology and Oceanography 34: 474-478.
46. Robblee MB, Barber TR, Carlson PR Jr, Durako MJ, Fourqurean JW, Muehlstein LK, Prorter D, Yarbro LA, Zieman RT, Zieman JC. 1991. Mass mortality of the tropical seagrass Thalassia testudinum in Florida Bay (USA). Marine Ecology Progress Series 71: 297-299.
47. Sand-Jensen K, Pedersen O, Binzer T, Borum J. 2005. Contrasting oxygen dynamics in the freshwater isoetid Lobelia dortmanna and the marine seagrass Zostera marina. Annals of Botany 96: 613-623.
48. Seddon S, Connolly R, Edyvane KS. 2000. Large-scale seagrass dieback in northern Spencer Gulf, South Australia. Aquatic Botany 66: 297-310.
49. Short FT, Duarte CM. 2001. Methods for the measurement of seagrass growth and production. In: Short FT, Coles RG, eds. Global seagrass research methods. Amsterdam, the Netherlands: Elsevier, 155-182.
50. Steen-Knudsen O. 2002. Biological membranes: theory of transport, potentials and electric impulses. Cambridge, UK: Cambridge University Press.
51. Truong DH, Eghbal MA, Hindmarsh W, Roth SH, O'Brien PJ. 2006. Molecular mechanisms of hydrogen sulfide toxicity. Drug Metabolism Reviews 38: 733-744.
52. Waycott M, Duarte CM, Carruthers TJB, Orth RJ, Dennison WC, Olyarnik S, Calladine A, Fourqurean JW, Heck KL Jr, Hughes AR et al. 2009. Accelerating loss of seagrasses across the globe threatens coastal ecosystems. Proceedings of the National Academy of Sciences, USA 106: 12377-12381.
53. Zieman JC, Fourqurean JW, Frankovich TA. 1999. Seagrass die-off in Florida Bay: long-term trends in abundance and growth of turtle grass, Thalassia testudinum. Estuaries 22: 460-470.