Effects of nutrient load on microbial activities within a seagrass-dominated ecosystem: Implications of changes in seagrass blue carbon

Marine Pollution Bulletin

Volumn 117, Issue 1-2, 2017, Pages 214-221

  Liu, Songlin ^a,b   Jiang, Zhijian ^a   Wu, Yunchao ^a,b   Zhang, Jingping ^a   Arbi, Iman ^a,b   Ye, Feng ^c   Huang, Xiaoping ^a,b   Macreadie, Peter Ian ^d  

^a SOUTH CHINA SEA INSTITUTE OF OCEANOLOGY   (China)

^b UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

^c GUANGZHOU INSTITUTE OF GEOCHEMISTRY   (China)

^d DEAKIN UNIVERSITY   (Australia)

Author keywords

Extracellular enzymes activities; Microbial community structure; PLFA; Seagrass bed; Sediment organic carbon; 13C

Indexed keywords

BACTERIA; ENZYME ACTIVITY; NUTRIENTS; ORGANIC CARBON; PLANTS (BOTANY); SEDIMENTS;

EXTRACELLULAR ENZYMES; MICROBIAL COMMUNITY STRUCTURES; PLFA; SEAGRASSES; SEDIMENT ORGANIC CARBON;

LOADING;

BETA FRUCTOFURANOSIDASE; CATECHOL OXIDASE; CELLULASE; FATTY ACID; SEA WATER; CARBON;

COMMUNITY STRUCTURE; DOMINANCE; ECOSYSTEM DYNAMICS; ENZYME ACTIVITY; MACROALGA; MARINE SEDIMENT; MICROBIAL ACTIVITY; MICROBIAL COMMUNITY; NUTRIENT CYCLING; ORGANIC CARBON; SEAGRASS;

ANALYTICAL PARAMETERS; ARTICLE; BACTERIUM; CARBON CYCLING; CARBON NITROGEN RATIO; CHINA; CONTROLLED STUDY; ELECTRIC CONDUCTIVITY; ENZYME ACTIVITY; FUNGUS; MICROBIAL ACTIVITY; MICROBIAL BIOMASS; MICROBIAL BIOMASS CARBON; MICROBIAL COMMUNITY; NONHUMAN; NUTRIENT; NUTRIENT LOADING; PH; SAND; SEAGRASS; SEDIMENT; SEDIMENT ORGANIC CARBON; ANIMAL; AQUACULTURE; BIOMASS; ECOSYSTEM; METABOLISM; MICROBIOLOGY; POACEAE; SEA;

CHINA; HAINAN; PACIFIC OCEAN; SOUTH CHINA SEA; XINCUN BAY;

ALGAE; FUNGI;

ANIMALS; AQUACULTURE; BACTERIA; BIOMASS; CARBON; CHINA; ECOSYSTEM; GEOLOGIC SEDIMENTS; OCEANS AND SEAS; POACEAE; WATER MICROBIOLOGY;

EID: 85011556279     PISSN: 0025326X     EISSN: 18793363     Source Type: Journal    
DOI: 10.1016/j.marpolbul.2017.01.056     Document Type: Article

References (67)

1. Abraham, W.-R., Hesse, C., Isotope fractionations in the biosynthesis of cell components by different fungi: a basis for environmental carbon flux studies. FEMS Microbiol. Ecol. 46 (2003), 121–128.
2. Alvarenga, P., Palma, P., Gonçalves, A.P., Baião, N., Fernandes, R.M., de Varennes, A., Vallini, G., Duarte, E., Cunha-Queda, A.C., Assessment of chemical, biochemical and ecotoxicological aspects in a mine soil amended with sludge of either urban or industrial origin. Chemosphere 72 (2008), 1774–1781.
3. Apostolaki, E., Holmer, M., Marbà, N., Karakassis, I., Metabolic imbalance in coastal vegetated (Posidonia oceanica) and unvegetated benthic ecosystems. Ecosystems 13 (2010), 459–471.
4. Bååth, E., The use of neutral lipid fatty acids to indicate the physiological conditions of soil fungi. Microb. Ecol. 45 (2003), 373–383.
5. Banta, G.T., Pedersen, M.F., Nielsen, S.L., Decomposition of marine primary producers: consequences for nutrient recycling and retention in coastal ecosystems. Nielsen, S.L., Banta, G.T., Pedersen, M.F., (eds.) Estuarine Nutrient Cycling: The Influence of Primary Producers, 2004, Kluwer Academic Publishers, Dordrecht, 187–216.
6. Boschker, H.T.S., de Brouwer, J.F.C., Cappenberg, T.E., The contribution of macrophyte-derived organic matter to microbial biomass in salt-marsh sediments: stable carbon isotope analysis of microbial biomarkers. Limnol. Oceanogr. 44 (1999), 309–319.
7. Boschker, H.T.S., Wielemaker, A., Schaub, B.E.M., Holmer, M., Limited coupling of macrophyte production and bacterial carbon cycling in the sediments of Zostera spp. meadows. Mar. Ecol. Prog. Ser. 203 (2000), 181–189.
8. Bossio, D.A., Scow, K.M., Impacts of carbon and flooding on soil microbial communities: phospholipid fatty acid profiles and substrate utilization patterns. Microb. Ecol. 35 (1998), 265–278.
9. Bouillon, S., Boschker, H.T.S., Bacterial carbon sources in coastal sediments: a cross-system analysis based on stable isotope data of biomarkers. Biogeosciences 3 (2006), 175–185.
10. Burkholder, J.M., Tomasko, D.A., Touchette, B.W., Seagrasses and eutrophication. J. Exp. Mar. Biol. Ecol. 350 (2007), 46–72.
11. Carlsson, A.S., van Beilen, J.B., Möller, R., Clayton, D., Micro- and Macro-algae: Utility for Industrial Applications. 2007, CPL Press, UK.
12. Cebrian, J., Patterns in the fate of production in plant communities. Am. Nat. 154 (1999), 449–468.
13. Chambers, L.G., Guevara, R., Boyer, J.N., Troxler, T.G., Davis, S.E., Effects of salinity and inundation on microbial community structure and function in a mangrove peat soil. Wetlands 36 (2016), 361–371.
14. Cheng, X., Luo, Y., Su, B., Zhou, X., Niu, S., Sherry, R., Weng, E., Zhang, Q., Experimental warming and clipping altered litter carbon and nitrogen dynamics in a tallgrass prairie. Agric. Ecosyst. Environ. 138 (2010), 206–213.
15. Chiu, S.-H., Huang, Y.-H., Lin, H.-J., Carbon budget of leaves of the tropical intertidal seagrass Thalassia hemprichii. Estuar. Coast. Shelf Sci. 125 (2013), 27–35.
16. Danovaro, R., Fabiano, M., Boyer, M., Seasonal changes of benthic bacteria in a seagrass bed (Posidonia oceanica) of the Ligurian Sea in relation to origin, composition and fate of the sediment organic matter. Mar. Biol. 119 (1994), 489–500.
17. Deforest, J.L., Zak, D.R., Pregitzer, K.S., Burton, A.J., Atmospheric nitrate deposition, microbial community composition, and enzyme activity in northern hardwood forests. Soil Sci. Soc. Am. J. 68 (2004), 132–138.
18. Duarte, C.M., Kennedy, H., Marbà, N., Hendriks, I., Assessing the capacity of seagrass meadows for carbon burial: current limitations and future strategies. Ocean Coast. Manag. 83 (2013), 32–38.
19. Fourqurean, J.W., Duarte, C.M., Kennedy, H., Marbà, N., Holmer, M., Mateo, M.A., Apostolaki, E.T., Kendrick, G.A., Krause-Jensen, D., McGlathery, K.J., Serrano, O., Seagrass ecosystems as a globally significant carbon stock. Nat. Geosci. 5 (2012), 505–509.
20. Freeman, C., Ostle, N., Kang, H., An enzymic ‘latch’ on a global carbon store. Nature, 409, 2001, 149.
21. Frostegård, A., Bååth, E., The use of phospholipid fatty acid analysis to estimate bacterial and fungal biomass in soil. Biol. Fertil. Soils 22 (1996), 59–65.
22. Green, E.P., Short, F.T., (eds.) World Atlas of Seagrasses, 2003, University of California Press, Berkeley.
23. Green, L., Lapointe, B.E., Gawlik, D.E., Winter nutrient pulse and seagrass epiphyte bloom: evidence of anthropogenic enrichment or natural fluctuations in the lower Florida Keys?. Estuar. Coasts 38 (2015), 1854–1871.
24. Greiner, J.T., McGlathery, K.J., Gunnell, J., McKee, B.A., Seagrass restoration enhances “blue carbon” sequestration in coastal waters. PLoS One, 8, 2013, e72469, 10.1371/journal.pone.0072469.
25. Guan, S., Soil Enzyme and Research Method. 1986, Agricultural Press, Beijing (in Chinese).
26. Hammel, K., Fungal degradation of lignin. Cadisch, G., Giller, K.E., (eds.) Driven by Nature: Plant Litter Quality and Decomposition, 1997, CAB International, Wallingford, 33–46.
27. Hauxwell, J., Valiela, I., Effects of nutrient loading on shallow seagrass-dominated coastal systems: patterns and processes. Nielsen, S.L., Banta, G.T., Pedersen, M.F., (eds.) Estuarine Nutrient Cycling: The Influence of Primary Producers, 2004, Kluwer Academic Publishers, Dordrecht, 59–92.
28. Hill, R., Bellgrove, A., Macreadie, P.I., Petrou, K., Beardall, J., Steven, A., Ralph, P.J., Can macroalgae contribute to blue carbon? An Australian perspective. Limnol. Oceanogr. 60 (2015), 1689–1706.
29. Holmer, M., Andersen, F.Ø., Nielsen, S.L., Boschker, H.T.S., The importance of mineralization based on sulfate reduction for nutrient regeneration in tropical seagrass sediments. Aquat. Bot. 71 (2001), 1–17.
30. Holmer, M., Duarte, C.M., Boschker, H.T.S., Barrón, C., Carbon cycling and bacterial carbon sources in pristine and impacted Mediterranean seagrass sediments. Aquat. Microb. Ecol. 36 (2004), 227–237.
31. Huang, X., Huang, L., Li, Y., Xu, Z., Fong, C., Huang, D., Han, Q., Huang, H., Tan, Y., Liu, S., Main seagrass beds and threats to their habitats in the coastal sea of South China. Chin. Sci. Bull. 51 (2006), 136–142.
32. Huang, X., Liu, S., Wang, H., Hu, Z., Li, Z., You, Y., Changes of soil microbial biomass carbon and community composition through mixing nitrogen-fixing species with Eucalyptus urophylla in subtropical China. Soil Biol. Biochem. 73 (2014), 42–48.
33. Jones, W.B., Cifuentes, L.A., Kaldy, J.E., Stable carbon isotope evidence for coupling between sedimentary bacteria and seagrasses in a sub-tropical lagoon. Mar. Ecol. Prog. Ser. 255 (2003), 15–25.
34. Karaca, A., Cetin, S.C., Turgay, O.C., Kizilkaya, R., Soil enzymes as indication of soil quality. Shukla, G., Varma, A., (eds.) Soil Enzymology, 2011, Springer-Verlag, Berlin, Heidelberg, 119–148.
35. Kiswara, W., Behnke, N., van Avesaath, P., Huiskes, A.H.L., Erftemeijer, P.L.A., Bouma, T.J., Root architecture of six tropical seagrass species, growing in three contrasting habitats in Indonesian waters. Aquat. Bot. 90 (2009), 235–245.
36. Kohl, L., Laganière, J., Edwards, K.A., Billings, S.A., Morrill, P.L., Van Biesen, G., Ziegler, S.E., Distinct fungal and bacterial δ13C signatures as potential drivers of increasing δ13C of soil organic matter with depth. Biogeochemistry 124 (2015), 13–26.
37. Lavery, P.S., McMahon, K., Weyers, J., Boyce, M.C., Oldham, C.E., Release of dissolved organic carbon from seagrass wrack and its implications for trophic connectivity. Mar. Ecol. Prog. Ser. 494 (2013), 121–133.
38. Lee, S., Oh, Y., Kim, D., Kwon, D., Lee, C., Lee, J., Converting carbohydrates extracted from marine algae into ethanol using various ethanolic Escherichia coli strains. Appl. Biochem. Biotechnol. 164 (2011), 878–888.
39. Li, X., Hou, L., Liu, M., Lin, X., Li, Y., Li, S., Primary effects of extracellular enzyme activity and microbial community on carbon and nitrogen mineralization in estuarine and tidal wetlands. Appl. Biochem. Biotechnol. 99 (2015), 2895–2909.
40. Liu, S., Jiang, Z., Zhang, J., Wu, Y., Lian, Z., Huang, X., Effect of nutrient enrichment on the source and composition of sediment organic carbon in tropical seagrass beds in the South China Sea. Mar. Pollut. Bull. 110 (2016), 274–280.
41. López, N.I., Duarte, C.M., Vallespinós, F., Romero, J., Alcoverro, T., The effect of nutrient additions on bacterial activity in seagrass (Posidonia oceanica) sediments. J. Exp. Mar. Biol. Ecol. 224 (1998), 155–166.
42. Lu, R., Analysis Methods of Soil and Agro-chemistry. 1999, China Agriculture Press, Beijing (in Chinese).
43. Macreadie, P.I., Allen, K., Kelaher, B.P., Ralph, P.J., Skilbeck, C.G., Paleoreconstruction of estuarine sediments reveal human-induced weakening of coastal carbon sinks. Glob. Chang. Biol. 18 (2012), 891–901.
44. Macreadie, P.I., Baird, M.E., Trevathan-Tackett, S.M., Larkum, A.W.D., Ralph, P.J., Quantifying and modelling the carbon sequestration capacity of seagrass meadows-a critical assessment. Mar. Pollut. Bull. 83 (2014), 430–439.
45. Malik, A.A., Chowdhury, S., Schlager, V., Oliver, A., Puissant, J., Vazquez, P.G.M., Jehmlich, N., von Bergen, M., Griffiths, R.I., Gleixner, G., Soil fungal: bacterial ratios are linked to altered carbon cycling. Front. Microbiol., 7, 2016, 1247, 10.3389/fmicb.2016.01247.
46. Mateo, M.A., Cebrián, J., Dunton, K., Mutchler, T., Carbon flux in seagrass ecosystems. Larkum, A.W.D., Orth, R.J., Duarte, C.M., (eds.) Seagrasses: Biology, 2006, Ecology and Conservation. Springer, Dordrecht, 159–192.
47. Parnell, A.C., Inger, R., Bearhop, S., Jackson, A.L., Source partitioning using stable isotopes: coping with too much variation. PLoS One, 5, 2010, e9672, 10.1371/journal.pone.0009672.
48. Sayer, E.J., Heard, M.S., Grant, H.K., Marthews, T.R., Tanner, E.V.J., Soil carbon release enhanced by increased tropical forest litterfall. Nat. Clim. Chang. 1 (2011), 304–307.
49. Schutter, M.E., Dick, R.P., Comparison of fatty acid methyl ester (FAME) methods for characterizing microbial communities. Soil Sci. Soc. Am. J. 64 (2000), 1659–1668.
50. Shao, X., Yang, W., Wu, M., Seasonal dynamics of soil labile organic carbon and enzyme activities in relation to vegetation types in Hangzhou bay tidal flat wetland. PLoS One, 10, 2015, e0142677, 10.1371/journal.pone.0142677.
51. Six, J., Frey, S.D., Thiet, R.K., Batten, K.M., Bacterial and fungal contributions to carbon sequestration in agroecosystems. Soil Sci. Soc. Am. J. 70 (2006), 555–569.
52. Song, Y., Song, C., Yang, G., Miao, Y., Wang, J., Guo, Y., Changes in labile organic carbon fractions and soil enzyme activities after marshland reclamation and restoration in the Sanjiang Plain in Northeast China. Environ. Manag. 50 (2012), 418–426.
53. Sparling, G.P., Ratio of microbial biomass carbon to soil organic carbon as a sensitive indicator of changes in soil organic matter. Aust. J. Soil Res. 30 (1992), 195–207.
54. Stemmer, M., Gerzabek, M.H., Kandeler, E., Organic matter and enzyme activity in particle-size fractions of soils obtained after low-energy sonication. Soil Biol. Biochem. 30 (1998), 9–17.
55. Touchette, B.W., Burkholder, J.M., Carbon and nitrogen metabolism in the seagrass, Zostera marina L.: environmental control of enzymes involved in carbon allocation and nitrogen assimilation. J. Exp. Mar. Biol. Ecol. 350 (2007), 216–233.
56. Trevathan-Tackett, S.M., Kelleway, J., Macreadie, P.I., Beardall, J., Ralph, P., Bellgrove, A., Comparison of marine macrophytes for their contributions to blue carbon sequestration. Ecology 96 (2015), 3043–3057.
57. Vance, E.D., Brookes, P.C., Jenkinson, D.S., An extraction method for measuring soil microbial biomass-C. Soil Biol. Biochem. 19 (1987), 703–707.
58. Volkman, J.K., Revill, A.T., Holdsworth, D.G., Fredericks, D., Organic matter sources in an enclosed coastal inlet assessed using lipid biomarkers and stable isotopes. Org. Geochem. 39 (2008), 689–710.
59. Waldrop, M.P., Zak, D.R., Sinsabaugh, R.L., Gallo, M., Lauber, C., Nitrogen deposition modifies soil carbon storage through changes in microbial enzymatic activity. Ecol. Appl. 14 (2004), 1172–1177.
60. Waycott, M., Duarte, C.M., Carruthers, T.J.B., Orth, R.J., Dennison, W.C., Olyarnik, S., Calladine, A., Fourqurean, J.W., Heck, K.L., Hughes, A.R., Kendrick, G.A., Kenworthy, W.J., Short, F.T., Williams, S.L., Accelerating loss of seagrasses across the globe threatens coastal ecosystems. Proc. Natl. Acad. Sci. U. S. A. 106 (2009), 12377–12381.
61. Yang, W., Zhao, H., Chen, X., Yin, S., Cheng, X., An, S., Consequences of short-term C4 plant Spartina alterniflora invasions for soil organic carbon dynamics in a coastal wetland of Eastern China. Ecol. Eng. 61 (2013), 50–57.
62. Yin, R., Deng, H., Wang, H.L., Zhang, B., Vegetation type affects soil enzyme activities and microbial functional diversity following re-vegetation of a severely eroded red soil in sub-tropical China. Catena 115 (2014), 96–103.
63. Zelles, L., Fatty acid patterns of phospholipids and lipopolysaccharides in the characterisation of microbial communities in soil: a review. Biol. Fertil. Soils 29 (1999), 111–129.
64. Zhang, C., Liu, G., Xue, S., Song, Z., Rhizosphere soil microbial activity under different vegetation types on the Loess Plateau, China. Geoderma 161 (2011), 115–125.
65. Zhang, J., Huang, X., Jiang, Z., Physiological responses of the seagrass Thalassia hemprichii (Ehrenb.) Aschers as indicators of nutrient loading. Mar. Pollut. Bull. 83 (2014), 508–515.
66. Ziegler, S., Benner, R., Nutrient cycling in the water column of a subtropical seagrass meadow. Mar. Ecol. Prog. Ser. 188 (1999), 51–62.
67. Ziegler, S., Kaiser, E., Benner, R., Dynamics of dissolved organic carbon, nitrogen and phosphorus in a seagrass meadow of Laguna Madre, Texas. Bull. Mar. Sci. 75 (2004), 391–407.