Skip to main content

Advertisement

Log in

Changes in Sediment Bacterial Community in Response to Long-Term Nutrient Enrichment in a Subtropical Seagrass-Dominated Estuary

  • Microbiology of Aquatic Systems
  • Published:
Microbial Ecology Aims and scope Submit manuscript

Abstract

Florida Bay exhibits a natural gradient of strong P limitation in the east which shifts to weak P or even N limitation at the western boundary. This nutrient gradient greatly affects seagrass abundance and productivity across the bay. We assessed the effects of N and P additions on sediment bacterial community structure in relation to the existing nutrient gradient in Florida Bay. Sediment samples from 24 permanent 0.25 m2 plots in each of six sites across Florida Bay were fertilized with granular N and P in a factorial design for 26 months. Sediment bacterial community structure was analyzed using PCR-denaturing gradient gel electrophoresis (DGGE) analysis of 16S ribosomal RNA (rRNA) genes and a cloning strategy from DGGE bands. The phylogenetic positions of 16S rRNA sequences mostly fell into common members found in marine sediments such as sulfate-reducing Deltaproteobacteria, Gammaproteobacteria, Spirochaetes, and Bacteriodetes. Twenty-eight common DGGE bands were found in all sediment samples; however, some DGGE bands were only found or were better represented in eastern sites. Bacterial community diversity (Shannon-Weiner index) showed similar values throughout all sediment samples. The N treatment had no effect on the bacterial community structures across the bay. Conversely, the addition of P significantly influenced the bacterial community structure at all but the most western site, where P is least limiting due to inputs from the Gulf of Mexico. P additions enhanced DGGE band sequences related to Cytophagales, Ectothiorhodospiraceae, and Desulfobulbaceae, suggesting a shift toward bacterial communities with increased capability to degrade polymeric organic matter. In addition, a band related to Deferribacteres was enhanced in eastern sites. Thus, indigenous environmental conditions were the primary determining factors controlling the bacterial communities, while the addition of P was a secondary determining factor. This P-induced change in community composition tended to be proportional to the amount of P limitation obviated by the nutrient additions.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  1. Nixon SW (1995) Coastal marine eutrophication: a definition, social causes, and future concerns. Ophelia 41:199–219

    Article  Google Scholar 

  2. Menzel DW, Hulburt EM, Ryther JH (1963) The effects of enriching Sargasso sea water on the production and species composition of the phytoplankton. Deep Sea Res Oceanogr Abstr 10:209–219

    Article  Google Scholar 

  3. Oviatt C, Lane P, French F, Donaghay P (1989) Phytoplankton species and abundance in response to eutrophication in coastal marine mesocosms. J Plankton Res 11:1223–1244

    Article  Google Scholar 

  4. Smith VH, Tilman GD, Nekola JC (1999) Eutrophication: impacts of excess nutrient inputs on freshwater, marine, and terrestrial ecosystems. Environ Pollut 100:179–196

    Article  CAS  PubMed  Google Scholar 

  5. Bowen JL, Crump BC, Deegan LA, Hobbie JE (2009) Increased supply of ambient nitrogen has minimal effect on salt marsh bacterial production. Limnol Oceanogr 54:713–722

    Article  CAS  Google Scholar 

  6. Flaten GAF, Castberg T, Tanaka T, Thingstad TF (2003) Interpretation of nutrient-enrichment bioassays by looking at sub-populations in a marine bacterial community. Aquat Microb Ecol 33:11–18

    Article  Google Scholar 

  7. Lebaron P, Servais P, Trossellier M, Courties C, Vives-Rego J, Muyzer G, Bernard L, Guindulain T, Shafer H, Stackenbrandt E (1999) Changes in bacterial community structure in seawater mesocosms differing in their nutrient status. Aquat Microb Ecol 19:255–267

    Article  Google Scholar 

  8. Pinhassi J, Gomez-Cosarnau L, Alonso-Saez L, Sala MM, Vidal M, Perdros-Alio C, Gasol JM (2006) Seasonal changes in bacterioplankton nutrient limitation and their effects on bacterial community composition in the NW Mediterranean Sea. Aquat Microb Ecol 44:241–252

    Article  Google Scholar 

  9. Sipura J, Hakka K, Helminen H, Lagus A, Suomela J, Sivonen K (2005) Effect of nutrient enrichment on bacterial biomass and community composition in mesocosms in the Archipelago Sea, northern Baltic. J Plankton Res 27:1261–1272

    Article  CAS  Google Scholar 

  10. Tuomi P, Fagerbakke KM, Bratbak G, Heldal M (1995) Nutritional enrichment of a microbial community: the effects on activity, elemental composition, community structure, and virus production. FEMS Microbiol Ecol 16:123–134

    Article  CAS  Google Scholar 

  11. Armitage AR, Frankovich TA, Heck KL Jr, Fourqurean JW (2005) Experimental nutrient enrichment causes complex changes in seagrass, microalgae, and macroalgae community structure in Florida Bay. Estuaries 28:422–434

    Article  Google Scholar 

  12. Duarte CM (1995) Submerged aquatic vegetation in relation to different nutrient regimes. Ophelia 41:87–112

    Article  Google Scholar 

  13. Ferdie M, Fourqurean JW (2004) Responses of seagrass communities to fertilization along a gradient of relative availability of nitrogen and phosphorus in a carbonate environment. Limnol Oceanogr 49:2082–2094

    Article  Google Scholar 

  14. Fourqurean JW, Powell GVN, Kenworthy WJ, Zieman JC (1995) The effects of long-term manipulation of nutrient supply on competition between the seagrasses Thalassia testudinum and Halodule wrightii in Florida Bay. Oikos 72:349–358

    Article  Google Scholar 

  15. Herbert DA, Fourqurean JW (2009) Phosphorus availability and salinity control productivity and demography of the seagrass Thalassia testudinum in Florida Bay. Estuar Coasts 32:188–201

    Article  CAS  Google Scholar 

  16. Karez R, Engelbert S, Kraufvelin P, Pedersen MF, Sommer U (2004) Biomass response and changes in composition of ephemeral macroalgal assemblages along an experimental gradient of nutrient enrichment. Aquat Bot 78:103–117

    Article  Google Scholar 

  17. McGlatherey KJ (2001) Macroalgal blooms contribute to the decline of seagrass in nutrient-enriched coastal waters. J Phycol 37:453–456

    Article  Google Scholar 

  18. Armitage AR, Frankovich TA, Fourqurean JW (2006) Variable responses within epiphytic and benthic microalgal communities to nutrient enrichment. Hydrobiologia 569:423–435

    Article  CAS  Google Scholar 

  19. Coleman VL, Burkholder JM (1994) Community structure and productivity of epiphytic microalgae on eelgrass (Zostera marina L.) under water-column nitrate enrichment. J Exp Mar Biol Ecol 179:29–48

    Article  Google Scholar 

  20. Hillebrand H, Sommer U (1997) Response of epilithic microphytobenthos of the Western Baltic Sea to in situ experiments with nutrient enrichment. Mar Ecol Prog Ser 160:35–46

    Article  Google Scholar 

  21. Pinckney J, Paerl HW, Fitzpatrick M (1995) Impacts of seasonality and nutrients on microbial mat community structure and function. Mar Ecol Prog Ser 123:207–216

    Article  Google Scholar 

  22. Sundback K, Snoeijs P (1991) Effects of nutrient enrichment on microalgal community composition in a coastal shallow water sediment system: an experimental study. Bot Mar 34:341–358

    Article  Google Scholar 

  23. Bowen JL, Ward BB, Morrison HG, Hobbie JE, Valiela I, Deegan LA, Sogin ML (2011) Microbial community composition in sediments resists perturbation by nutrient enrichment. ISME J 5:1540–1548

    Article  PubMed Central  PubMed  Google Scholar 

  24. Piceno YM, Lovell CR (2000) Stability in natural bacterial communities: II. Plant resource allocation effects on rhizosphere diazotroph assemblage composition. Microb Ecol 39:41–48

    Article  CAS  PubMed  Google Scholar 

  25. Nilsson P, Johnsson B, Swanberg IL, Sundback K (1991) Response of a marine shallow-water sediment system to an increased load of inorganic nutrients. Mar Ecol Prog Ser 71:275–290

    Article  Google Scholar 

  26. Lopez NI, Duarte CM, Vallespinos F, Romero J, Alcoverro T (1998) The effect of nutrient additions on bacterial activity in seagrass (Posidonia oceanica) sediments. J Exp Mar Biol Ecol 224:155–166

    Article  CAS  Google Scholar 

  27. Xu P, Leff LG (2004) Longitudinal changes in the benthic bacterial community of the Mahoning River (Ohio, U.S.A.). Hydrobiologia 522:329–335

    Article  Google Scholar 

  28. Bowman JP, McCammon SA, Gibson JAE, Robertson L, Nichols PD (2003) Prokaryotic activity and community structure in Antarctic continental shelf sediment. Appl Environ Microbiol 69:2448–2462

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  29. Bissett A, Bowman J, Burke C (2006) Bacterial diversity in organically-enriched fish farm sediments. FEMS Microbiol Ecol 55:48–56

    Article  CAS  PubMed  Google Scholar 

  30. Hewson I, Vargo GA, Fuhrman JA (2003) Bacterial diversity in shallow oligotrophic marine benthos and overlying waters: effects of virus infection, containment, and nutrient enrichment. Microb Ecol 46:322–336

    Article  CAS  PubMed  Google Scholar 

  31. Boyer JN, Fourqurean JW, Jones RD (1997) Spatial characterization of water quality in Florida Bay and Whitewater Bay by principal component and cluster analyses: zones of similar influence (ZSI). Estuaries 20:743–758

    Article  CAS  Google Scholar 

  32. Fourqurean JW, Zieman JG, Powell GVN (1992) Phosphorus limitation of primary production in Florida Bay: evidence from C:N:P ratios of the dominant seagrass Thalassia testudinum. Limnol Oceanogr 37:162–171

    Article  CAS  Google Scholar 

  33. Fourqurean JW, Jones RD, Zieman JC (1993) Processes influencing water column nutrient characteristics and phosphorus limitation of phytoplankton biomass in Florida Bay, USA: influences from spatial distributions. Estuar Coast Shelf Sci 36:295–314

    Article  CAS  Google Scholar 

  34. Lavrentyev PJ, Bootsma HA, Johengen TA, Cavaletto JF, Gardner WS (1998) Microbial plankton response to resource limitation: insight from the community structure and seston stoichiometry in Florida Bay, USA. Mar Ecol Prog Ser 165:45–57

    Article  CAS  Google Scholar 

  35. Phlips EJ, Badylak S (1996) Spatial variability in phytoplankton standing crop and composition in a shallow inner-shelf lagoon, Florida Bay, Florida. Bull Mar Sci 58:203–216

    Google Scholar 

  36. Tomas CR, Bendis B, Johns K (1999) Role of nutrients in regulating plankton blooms in Florida Bay. In: Kumpf H, Steidinger K, Sherman K (eds) The Gulf of Mexico large marine ecosystem. Blackwell Science, Malden, pp 323–337

    Google Scholar 

  37. Solorzano L, Sharp JH (1980) Determination of total dissolved nitrogen in natural waters. Limnol Oceanogr 25:751–754

    Article  CAS  Google Scholar 

  38. Bodelier PLE, Meima-Franke M, Zwart G, Laanbroek HJ (2005) New DGGE strategies for the analyses of methanotrophic microbial communities using different combinations of existing 16S rRNA-based primers. FEMS Microbiol Ecol 52:163–174

    Article  CAS  PubMed  Google Scholar 

  39. Coci M, Riechmann D, Bodelier PLE, Stefani S, Zwart G, Laanbroek HJ (2005) Effect of salinity on temporal and spatial dynamics of ammonia-oxidising bacteria from intertidal freshwater sediment. FEMS Microbiol Ecol 53:359–368

    Article  CAS  PubMed  Google Scholar 

  40. Crump BC, Kling GW, Bahr M, Hobbie JE (2003) Bacterioplankton community shifts in an Arctic lake correlate with seasonal changes in organic matter source. Appl Environ Microbiol 69:2253–2268

    Article  PubMed Central  PubMed  Google Scholar 

  41. Crump BC, Hopkinson CS, Sogin ML, Hobbie JE (2004) Microbial biogeography along an estuarine salinity gradient: combined influences of bacterial growth and residence time. Appl Environ Microbiol 70:1494–1505

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  42. Köpke B, Wilms R, Engelen B, Cypionka H, Sass H (2005) Microbial diversity in coastal subsurface sediments: a cultivation approach using various electron acceptors and substrate gradients. Appl Environ Microbiol 71:7819–7830

    Article  PubMed Central  PubMed  Google Scholar 

  43. Muyzer G, de Waal EC, Uitterlinden AG (1993) Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA. Appl Environ Microbiol 59:695–700

    PubMed Central  CAS  PubMed  Google Scholar 

  44. Parkes RJ, Cragg BA, Banning N, Brock F, Webster G, Fry JC, Hornibrook E, Pancost RD, Kelly S, Knab N, Jørgensen BB, Rinna J, Weightman AJ (2007) Biogeochemistry and biodiversity of methane cycling in subsurface marine sediments (Skagerrak, Denmark). Environ Microbiol 9:1146–1161

    Article  CAS  PubMed  Google Scholar 

  45. Templer SP, Wehrmann LM, Zhang Y, Vasconcelos C, McKenzie JA (2011) Microbial community composition and biogeochemical processes in cold-water coral carbonate mounds in the Gulf of Cadiz, on the Moroccan margin. Mar Geol 282:138–148

    Article  CAS  Google Scholar 

  46. Webster G, Newberry CJ, Fry JC, Weightman AJ (2003) Assessment of bacterial community structure in the deep sub-seafloor biosphere by 16S rDNA-based techniques: a cautionary tale. J Microbiol Methods 55:155–164

    Article  CAS  PubMed  Google Scholar 

  47. Webster G, Parkes RJ, Cragg BA, Newberry CJ, Weightman AJ, Fry JC (2006) Prokaryotic community composition and biogeochemical processes in deep subseafloor sediments from the Peru Margin. FEMS Microbiol Ecol 58:65–85

    Article  CAS  PubMed  Google Scholar 

  48. Zeng J, Yang L, Li J, Liang Y, Xiao L, Jiang L, Zhao D (2009) Vertical distribution of bacterial community structure in the sediments of two eutrophic lakes revealed by denaturing gradient gel electrophoresis (DGGE) and multivariate analysis techniques. World J Microbiol Biotechnol 25:225–233

    Article  CAS  Google Scholar 

  49. Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98

    CAS  Google Scholar 

  50. Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  51. Swofford DL (2006) PAUP: phylogenetic analysis using parsimony. Macintosh Beta v. 10. Sinauer Associates, Sunderland, Mass

  52. Hood GM (2008) PopTools: version 3.0.6. Available on the internet. URL: http://www.cse.csiro.au/poptools/

  53. Zieman JC, Fourqurean JW, Iverson RL (1989) Distribution, abundance and productivity of seagrass and macroalgae in Florida Bay. Bull Mar Sci 44:292–311

    Google Scholar 

  54. Ikenaga M, Guevara R, Dean AL, Pisani C, Boyer JN (2010) Changes in community structure of sediment bacteria along the Florida Coastal Everglades marsh–mangrove–seagrass salinity gradient. Microb Ecol 59:284–295

    Article  PubMed  Google Scholar 

  55. Ravenschlag K, Sahm K, Pernthaler J, Amann R (1999) High bacterial diversity in permanently cold marine sediments. Appl Environ Microbiol 65:3982–3989

    PubMed Central  CAS  PubMed  Google Scholar 

  56. Cifuentes A, Antón J, Benlloch S, Donnelly A, Herbert RA, Rodríguez-Valera F (2000) Prokaryotic diversity in Zostera noltii-colonized marine sediments. Appl Environ Microbiol 66:1715–1719

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  57. Bowman JP, McCuaig RD (2003) Biodiversity, community structural shifts, and biogeography of prokaryotes within Antarctic continental shelf sediment. Appl Environ Microbiol 69:2463–2483

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  58. Gray J, Herwig RP (1996) Phylogenetic analysis of the bacterial communities in marine sediments. Appl Environ Microbiol 63:4049–4059

    Google Scholar 

  59. Asami H, Aida M, Watanabe K (2005) Accelerated sulfur cycle in coastal marine sediment beneath areas of intensive shellfish aquaculture. Appl Environ Microbiol 71:2925–2933

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  60. Li H, Yu Y, Luo W, Zeng Y, Chen B (2009) Bacterial diversity in surface sediments from the Pacific Arctic Ocean. Extremophiles 13:233–246

    Article  CAS  PubMed  Google Scholar 

  61. Ward AC, Bora N (2006) Diversity and biogeography of marine actinobacteria. Curr Opin Microbiol 9:279–286

    Article  CAS  PubMed  Google Scholar 

  62. Lasher C, Dyszynskin G, Everett K, Edmonds J, Ye W, Sheldon W, Wang S, Joye SB, Moran MA, Whitman WB (2009) The diverse bacterial community in intertidal, anaerobic sediments at Sapelo Island, Georgia. Microb Ecol 58:244–261

    Article  PubMed Central  PubMed  Google Scholar 

  63. Jensen S, Neufeld JD, Birkeland NK, Hovland M, Murrell JC (2008) Insight into the microbial community structure of a Norwegian deep-water coral reef environment. Deep Sea Res I 55:1554–1563

    Article  Google Scholar 

  64. Piza FF, Prado PI, Manfio GP (2004) Investigation of bacterial diversity in Brazilian tropical estuarine sediments reveals high actinobacterial diversity. Antonie Van Leeuwenhoek 86:317–328

    Article  CAS  PubMed  Google Scholar 

  65. Sørensen KB, Glazer B, Hannides A, Gaidos E (2007) Spatial structure of the microbial community in sandy carbonate sediment. Mar Ecol Prog Ser 346:61–74

    Article  Google Scholar 

  66. Holt JG, Krieg NR, Sneath PHA, Staley JT, Williams ST (eds) (1994) Bergey’s manual of determinative bacteriology, 9th edn. Lippincott Williams and Wilkins, Baltimore

    Google Scholar 

  67. Reichenbach H et al (1992) The order Cytophagales. In: The prokaryotes. Springer-Verlag, New York, pp 3631–3675

    Chapter  Google Scholar 

  68. Reichenbach H, Dworkin M (1992) The Myxobacteria. In: Balows A, Truper HG, Dworkin M, Harder W, Schleifer KH (eds) The prokaryotes. Springer-Verlag, New York, pp 3416–3487

    Chapter  Google Scholar 

  69. Venter JC, Remington K, Heidelberg JF, Halpern AL, Rusch D, Eisen JA, Wu D, Paulsen I, Nelson KE, Nelson W, Fouts DE, Levy S, Knap AH, Lomas MW, Nealson K, White O, Peterson J, Hoffman J, Parsons R, Baden-Tillson H, Pfannkoch C, Rogers YH, Hamilton O, Smith HO (2004) Environmental genome shotgun sequencing of the Sargasso Sea. Science 304:66–74

    Article  CAS  PubMed  Google Scholar 

  70. Uthicke S, McGuire K (2007) Bacterial communities in Great Barrier Reef calcareous sediments: contrasting 16S rDNA libraries from nearshore and outer shelf reefs. Estuar Coast Mar Sci 72:188–200

    Article  Google Scholar 

  71. Jasti S, Sieracki ME, Poulton NJ, Giewat MW, Rooney-Varga JN (2005) Phylogenetic diversity and specificity of bacteria closely associated with Alexandrium spp. and other phytoplankton. Appl Environ Microbiol 71:3483–3494

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  72. Krick A, Kehraus S, Eberl L, Riedel K, Anke H, Kaesler I, Graeber I, Szewzyk U, König GM (2007) A marine Mesorhizobium sp. produces structurally novel long-chain N-acyl-L-homoserine lactones. Appl Environ Microbiol 73:3587–3594

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  73. Tamminen M, Karkman A, Corander J, Paulin L, Virta M (2011) Differences in bacterial community composition in Baltic Sea sediment in response to fish farming. Aquaculture 313:15–23

    Article  Google Scholar 

  74. Sorokin DY, Lysenko AM, Mityushina LL, Tourova TP, Jones BE, Rainey FA, Robertson LA, Kuenen GJ (2001) Thioalkalimicrobium aerophilum gen. nov., sp. nov. and Thioalkalimicrobium sibericum sp. nov., and Thioalkalivibrio versutus gen. nov., sp. nov., Thioalkalivibrio nitratis sp. nov. and Thioalkalivibrio denitrificans sp. nov., novel obligately alkaliphilic and obligately chemolithoautotrophic sulfur-oxidizing bacteria from soda lakes. Int J Syst Evol Microbiol 51:565–580

    Article  CAS  PubMed  Google Scholar 

  75. Koike I, Sorensen J (1988) Nitrate reduction and denitrification in marine sediments. In: Blackbum TH, Sorensen J (eds) Nitrogen cycling in coastal marine environments. John Wiley & Sons, pp 251–273

  76. Holmes B (1992) The genera Flavobacterium, Spingobacterium, and Weeksella. In: Balows A, Truper HG, Dworkin M, Harder W, Schleifer KH (eds) The prokaryotes. Springer-Verlag, New York, pp 3620–3630

    Chapter  Google Scholar 

  77. Whitton A, Potts M (2000) Introduction to the Cyanobacteria. In: Whitton A, Potts M (eds) The ecology of cyanobacteria: their diversity in time and space. Kluwer Academic Publishers, Dordrecht, pp 1–11

    Google Scholar 

  78. Mir J, Martínez-Alonso M, Caumette P, Guerrero R, Esteve I (2002) Sulfide fluxes in a microbial mat from the Ebro Delta, Spain. Int Microbiol 5:133–138

    Article  CAS  PubMed  Google Scholar 

  79. Martínez-Alonso M, Bleijswijk JV, Gaju N, Muyzer G (2005) Diversity of anoxygenic phototrophic sulfur bacteria in the microbial mats of the Ebro Delta: a combined morphological and molecular approach. FEMS Microbiol Ecol 52:339–350

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

We wish to thank Jim Fourqurean and Anna Armitage for their permission to sample their field plots and for their ongoing support and suggestions. This research was supported by the National Science Foundation through the Florida Coastal Everglades Long-Term Ecological Research Program (DEB-9910514). This is contribution #667 of the Southeast Environmental Research Center at Florida International University.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Joseph N. Boyer.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Guevara, R., Ikenaga, M., Dean, A.L. et al. Changes in Sediment Bacterial Community in Response to Long-Term Nutrient Enrichment in a Subtropical Seagrass-Dominated Estuary. Microb Ecol 68, 427–440 (2014). https://doi.org/10.1007/s00248-014-0418-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00248-014-0418-1

Keywords

Navigation