Increased Variability of Microbial Communities in Restored Salt Marshes nearly 30 Years After Tidal Flow Restoration

Estuaries and Coasts

Volumn 35, Issue 4, 2012, Pages 1049-1059

  Bernhard, Anne E ^a   Marshall, David ^a   Yiannos, Lazaros ^a  

^a The Holleran Center for Community Action and Public Policy   (United States)

Author keywords

16S rRNA; Disturbance; Diversity; Impoundment; Long Island Sound; TRFLP

Indexed keywords

BACTERIUM; COMMUNITY COMPOSITION; DISTURBANCE; ECOSYSTEM RESILIENCE; GENETIC ANALYSIS; MICROBIAL COMMUNITY; SALTMARSH; SOIL MICROORGANISM; SPATIOTEMPORAL ANALYSIS; SPECIES DIVERSITY; TIDAL CYCLE;

LONG ISLAND SOUND; UNITED STATES;

BACTERIA (MICROORGANISMS); BACTEROIDETES; PLANCTOMYCETES; PROTEOBACTERIA;

EID: 84861907868     PISSN: 15592723     EISSN: 15592731     Source Type: Journal    
DOI: 10.1007/s12237-012-9502-2     Document Type: Article

References (64)

1. Allen, E. A., P. E. Fell, M. A. Peck, J. A. Gieg, C. R. Guthke, and M. D. Newkirk. 1994. Gut contents of common mummichogs, Fundulus heteroclitus L., in a restored impounded marsh and in natural reference marshes. Estuaries 17: 462-471.
2. Allison, S. D., and J. B. H. Martiny. 2008. Resistance, resilience, and redundancy in microbial communities. Proceedings of the National Academy of Sciences of the United States of America 105: 11512-11519.
3. Ayala-Del-Rio, H. L., S. J. Callister, C. S. Criddle, and J. M. Tiedje. 2004. Correspondence between community structure and function during succession in phenol- and phenol-plus-trichloroethene-fed sequencing batch reactors. Applied and Environmental Microbiology 70: 4950-4960.
4. Begon, M., J. L. Harper, and C. R. Townsend. 1990. Ecology: Individuals, populations and communities. Cambridge, MA: Blackwell.
5. Benoit, L. K., and R. S. Askins. 1999. Impact of the spread of Phragmites on the distribution of birds in Connecticut tidal marshes. Wetlands 19: 194-208.
6. Bernhard, A. E., D. Colbert, J. McManus, and K. G. Field. 2005a. Microbial community dynamics based on 16S rRNA gene profiles in a Pacific Northwest estuary and its tributaries. FEMS Microbiology Ecology 52: 115-128.
7. Bernhard, A. E., T. Donn, A. E. Giblin, and D. A. Stahl. 2005b. Loss of diversity of ammonia-oxidizing bacteria correlates with increasing salinity in an estuary system. Environmental Management 7: 1289-1297.
8. Bernhard, A. E., J. Tucker, A. E. Giblin, and D. A. Stahl. 2007. Functionally distinct communities of ammonia-oxidizing bacteria along an estuarine salinity gradient. Environmental Microbiology 9: 1439-1447.
9. Bordalo, A. A. 1993. Effects of salinity on bacterioplankton: Field and microcosm experiments. Journal of Applied Bacteriology 75: 393-398.
10. Bouvier, T. C., and P. A. del Giorgio. 2002. Compositional changes in free-living bacterial communities along a salinity gradient in two temperate estuaries. Limnology and Oceanography 47: 453-470.
11. Bowen, J. L., B. C. Crump, L. A. Deegan, and J. E. Hobbie. 2009. Salt marsh sediment bacteria: Their distribution and response to external nutrient inputs. ISME Journal 3: 924-934.
12. Brawley, A. H., R. S. Warren, and R. S. Askins. 1998. Bird use of restoration and reference marshes within the Barn Island Wildlife Management Area, Stonington, Connecticut, USA. Environmental Management 22: 625-633.
13. Collins, B., G. Wein, and T. Philippi. 2001. Effects of disturbance intensity and frequency on early old-field succession. Journal of Vegetation Science 12: 721-728.
14. Crain, G. M., K. B. Gedan, and M. Dionne. 2009. Tidal restrictions and mosquito ditching in New England marshes. In Human impacts on salt marshes: A global perspective, ed. B. R. Silliman, E. D. Grosholz, and M. D. Bertness. Berkeley, CA: University of California Press.
15. Crump, B. C., C. S. Hopkinson, M. L. Sogin, and J. E. Hobbie. 2004. Microbial biogeography along an estuarine salinity gradient: Combined influences of bacterial growth and residence time. Applied and Environmental Microbiology 70: 1494-1505.
16. Denslow, J. S. 1985. Disturbance-mediated coexistence of species. In The ecology of natural disturbance and patch dynamics, ed. S. T. A. Pickett and P. S. White. Orlando: Academic.
17. Dunbar, J., L. O. Ticknor, and C. R. Kuske. 2000. Assessment of microbial diversity in four southwestern United States soils by 16S rRNA gene terminal restriction fragment analysis. Applied and Environmental Microbiology 66: 2943-2950.
18. Fernandez, A. S., S. A. Hashsham, S. L. Dollhopf, L. Raskin, O. Glagoleva, F. B. Dazzo, R. F. Hickey, C. S. Criddle, and J. M. Tiedje. 2000. Flexible community structure correlates with stable community function in methanogenic bioreactor communities perturbed by glucose. Applied and Environmental Microbiology 66: 4058-4067.
19. Finlay, B. J., S. C. Maberly, and J. I. Cooper. 1997. Microbial diversity and ecosystem function. Oikos 80: 209-213.
20. Fraterrigo, J. M., and J. A. Rusak. 2008. Disturbance-driven changes in the variability of ecological patterns and processes. Ecology Letters 11: 756-770.
21. Fuerst, J. 1995. The Planctomycetes: Emerging models for microbial ecology, evolution and cell biology. Microbiology 141: 1493-1506.
22. Glockner, F. O., B. M. Fuchs, and R. Amann. 1999. Bacterioplankton compositions of lakes and oceans: A first comparison based on fluorescence in situ hybridization. Applied and Environmental Microbiology 65: 3721-3726.
23. Griffiths, B. S., H. L. Kuan, K. Ritz, L. A. Glover, A. E. McCaig, and C. Fenwick. 2004. The relationship between microbial community structure and functional stability, tested experimentally in an upland pasture soil. Microbial Ecology 47: 104-113.
24. Grman, E., J. A. Lau, D. R. Schoolmaster, and K. L. Gross. 2010. Mechanisms contributing to stability in ecosystem function depend on the environmental context. Ecology Letters 13: 1400-1410.
25. Hardwick, E. O., W. Ye, M. A. Moran, and R. E. Hodson. 2003. Temporal dynamics of three culturable γ-Proteobacteria taxa in salt marsh sediments. Aquatic Ecology 37: 55-64.
26. Hashsham, S. A., A. S. Fernandez, S. L. Dollhopf, F. B. Dazzo, R. F. Hickey, J. M. Tiedje, and C. S. Criddle. 2000. Parallel processing of substrate correlates with greater functional stability in methanogenic bioreactor communities perturbed by glucose. Applied and Environmental Microbiology 66: 4050-4057.
27. Herbert, D. A., and J. W. Fourqurean. 2008. Ecosystem structure and function still altered two decades after short-term fertilization of a seagrass meadow. Ecosystems 11: 688-700.
28. Holling, C. S. 1973. Resilience and stability of ecological systems. Annual Review of Ecology and Systematics 4: 1-23.
29. Könneke, M., A. E. Bernhard, J. R. de la Torre, C. B. Walker, J. B. Waterbury, and D. A. Stahl. 2005. Isolation of an autotrophic ammonia-oxidizing marine archaeon. Nature 437: 543-546.
30. Kruskal, J. B. 1964. Nonmetric multidimensional scaling: A numerical method. Psychometrika 29: 115-129.
31. Lane, D. J. 1991. 16S/23S rRNA sequencing. In Nuleic acid techniques in bacterial systematic, eds. E. Stackebrandt and M. Goodfellow. New York: Wiley.
32. Lane, D. J., B. Pace, G. J. Olsen, D. A. Stahl, M. L. Sogin, and N. R. Pace. 1985. Rapid determination of 16S ribosomal RNA sequences for phylogenetic analyses. Proceeding of the National Academy of Sciences of the United States of America 82: 6955-6959.
33. LaRiviere, D., R. L. Autenrieth, and J. S. Bonner. 2004. Redox dynamics of a tidally-influenced wetland on the San Jacinto River. Estuaries 27: 253-264.
34. Ludwig, W., O. Strunk, R. Westram, L. Richter, H. Meier, A. Yadhukumar, T. Buchner, S. Lai, G. Steppi, W. Jobb, I. Förster, S. Brettske, A. W. Gerber, O. Ginhart, S. Gross, S. Grumann, R. Hermann, A. Jost, T. König, R. Liss, M. Lüßmann, B. May, B. Nonhoff, R. Reichel, A. Strehlow, N. Stamatakis, A. Stuckmann, M. Vilbig, T. Lenke, A. B. Ludwig, and K.-H. Schleifer. 2004. ARB: A software environment for sequence data. Nucleic Acids Research 32: 1363-1371.
35. Maoz, A., R. Mayr, and S. Scherer. 2003. Temporal stability and biodiversity of two complex antilisterial cheese-ripening microbial consortia. Applied and Environmental Microbiology 69: 4012-4018.
36. McCune, B., and G. Cottam. 1985. The successional status of a southern Wisconsin oak woods. Ecology 66: 1270-1278.
37. McCune, B., and J. B. Grace. 2002. Analysis of ecological communities. Gleneden Beach, OR: MjM Software Design.
38. McCune, B., and M. J. Mefford. 1999. PC-ORD. Gleneden Beach, OR, MjM Software: Multivariate analysis of ecological data.
39. Miller, W. R., and F. E. Egler. 1950. Vegetation of the Wequetequock-Pawcatuck tidal marshes, Connecticut. Ecological Monographs 20: 143-172.
40. Moin, N. S., K. A. Nelson, A. Bush, and A. E. Bernhard. 2009. Distribution and diversity of archaeal and bacterial ammonia-oxidizers in salt marsh sediment. Applied and Environmental Microbiology 75: 7461-7468.
41. Naeem, S., and S. Li. 1997. Biodiversity enhances ecosystem reliability. Nature 390: 507-509.
42. Nielsen, J. L., A. Schramm, A. E. Bernhard, G. J. van Den Engh, and D. A. Stahl. 2004. Flow cytometry-assisted cloning of specific sequence motifs from complex 16S rRNA gene libraries. Applied and Environmental Microbiology 70: 7550-7554.
43. Odum, E. P. 1985. Trends expected in stressed ecosystems. BioScience 35: 419-422.
44. Oliveira, V., A. L. Santos, F. Coelho, N. C. M. Gomes, H. Silva, A. Almeida, and A. Cunha. 2010. Effects of monospecific banks of salt marsh vegetation on sediment bacterial communities. Microbial Ecology 60: 167-179.
45. Onaindia, M., I. Albizu, and I. Amezaga. 2001. Effect of time on the natural regeneration of salt marsh. Applied Vegetation Science 4: 247-256.
46. Peck, M. A., P. E. Fell, E. A. Allen, J. A. Gieg, C. R. Guthke, and M. D. Newkirk. 1994. Evaluation of tidal marsh restoration: Comparison of selected macroinvertebrate populations on a restored impounded valley marsh and an unimpounded valley marsh within the same system in Connecticut, USA. Environmental Management 18: 283-293.
47. Portnoy, J. W., and A. E. Giblin. 1997. Biogeochemical effects of seawater restoration to diked salt marshes. Ecological Applications 7: 1054-1063.
48. Ravit, B., J. G. Ehenfeld, and M. M. Haggblom. 2006. Effects of vegetation on root-associated microbial communities: A comparison of disturbed versus undisturbed estuarine sediments. Soil Biology and Biochemistry 38: 2359-2371.
49. Ravit, B., J. G. Ehrenfeld, M. M. Haggblom, and M. Bartels. 2007. The effects of drainage and nitrogen enrichment on Phragmites australis, Spartina alterniflora, and their root-associated microbial communities. Wetlands 27: 915-927.
50. Revilla, M., A. Iriarte, I. Madariaga, and E. Orive. 2000. Bacterial and phytoplankton dynamics along a trophic gradient in a shallow temperate estuary. Estuarine, Coastal and Shelf Science 50: 297-313.
51. Roman, C. T., K. B. Raposa, S. C. Adamowicz, M.-J. James-Pirri, and J. G. Catena. 2002. Quantifying vegetation and nekton response to tidal restoration of a New England salt marsh. Restoration Ecology 10: 450-460.
52. Santos, L., Ç. Cunha, H. Silva, I. Caçador, J. M. Dias, and A. Almeida. 2007. Influence of salt marsh on bacterial activity in two estuaries with different hydrodynamic characteristics (Ria de Aveiro and Tagus Estuary). FEMS Microbiology Ecology 60: 429-441.
53. Schloss, P. D. 2008. Evaluating different approaches that test whether microbial communities have the same structure. ISME Journal 2: 265-275.
54. Schloss, P. D., S. L. Westcott, T. Ryabin, J. R. Hall, M. Hartmann, E. B. Hollister, R. A. Lesniewski, B. B. Oakley, D. H. Parks, C. J. Robinson, J. W. Sahl, B. Stres, G. G. Thallinger, D. J. van Horn, and C. F. Weber. 2009. Introducing mothur: Open-source, platform-independent, community-supported software for describing and comparing microbial communities. Applied and Environmental Microbiology 75: 7537-7541.
55. Singleton, D. R., M. A. Furlong, S. L. Rathbun, and W. B. Whitman. 2001. Quantitative comparisons of 16S rRNA gene sequence libraries from environmental samples. Applied and Environmental Microbiology 67: 4374-4376.
56. Sinicrope, T. L., P. G. Hine, R. S. Warren, and W. A. Niering. 1990. Restoration of an impounded salt marsh in New England. Estuaries 13: 25-30.
57. Swamy, V., P. E. Fell, M. Body, M. B. Keaney, M. K. Nyaku, E. C. McIlvain, and A. L. Keen. 2002. Macroinvertebrate and fish populations in a restored impounded salt marsh 21 years after the reestablishment of tidal flooding. Environmental Management 29: 516-530.
58. Urbach, E., K. L. Vergin, L. Young, A. Morse, G. L. Larson, and S. J. Giovannoni. 2001. Unusual bacterioplankton community structure in ultra-oligotrophic Crater Lake. Limnology and Oceanography 46: 557-572.
59. Valentine, D. L. 2002. Biogeochemistry and microbial ecology of methane oxidation in anoxic environments: A review. Antonie van Leeuwenhoek 81: 271-282.
60. Wang, Q., G. M. Garrity, J. M. Tiedje, and J. R. Cole. 2007. Naïve Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Applied and Environmental Microbiology 73(16): 5261-5267.
61. Warren, R. S., and W. A. Neiring. 1993. Vegetation changes on a northeast tidal marsh: Interaction of sea-level rise and accretion. Ecology 74: 96-103.
62. Warren, R. S., P. E. Fell, J. L. Grimsby, E. L. Buck, G. C. Rilling, and R. A. Fertik. 2001. Rates, patterns, and impacts of Phragmites australis expansion and effects of experimental Phragmites control on vegetation, macroinvertebrates, and fish within tidelands of the lower Connecticut River. Estuaries 24: 90-107.
63. Warren, R. S., P. E. Fell, R. Rozsa, A. H. Brawley, A. C. Orsted, E. T. Olson, V. Swamy, and W. A. Niering. 2002. Salt marsh restoration in Connecticut: 20 years of science and management. Restoration Ecology 10: 497-513.
64. Zedler, J. B., and S. Kercher. 2005. Wetland resources: Status, trends, ecosystem services, and restorability. Annual Review of Environment and Resources 30: 39-74.