Abstract
Salt marshes are important ecosystems whose plant and microbial communities can alter terrestrially derived pollutants prior to coastal water discharge. However, knowledge regarding relationships between anthropogenic pollutant levels and salt marsh microbial communities is limited, and salt marshes on the West Coast of the United States are rarely examined. In this study, we investigated the relationships between microbial community composition and 24 pollutants (20 metals and 4 organics) in two California salt marshes. Multivariate ordination techniques were used to assess how bacterial community composition, as determined by terminal restriction fragment length polymorphism and phospholipid fatty acid analyses, was related to pollution. Sea urchin embryo toxicity measurements and plant tissue metabolite profiles were considered two other biometrics of pollution. Spatial effects were strongly manifested across marshes and across channel elevations within marshes. Utilizing partial canonical correspondence analysis, an ordination technique new to microbial ecology, we found that several metals were strongly associated with microbial community composition after accounting for spatial effects. The major patterns in plant metabolite profiles were consistent with patterns across microbial community profiles, but sea urchin embryo assays, which are commonly used to evaluate ecological toxicity, had no identifiable relationships with pollution. Whereas salt marshes are generally dynamic and complex habitats, microbial communities in these marshes appear to be relatively sensitive indicators of toxic pollutants.
Similar content being viewed by others
References
Bachoon, DS, Hodson, RE, Araujo, R (2001) Microbial community assessment in oil-impacted salt marsh sediment microcosms by traditional and nucleic acid-based indices. J Microbiol Methods 46: 37–49
Beasley, G, Kneale, PE (2003) Investigating the influence of heavy metals on macroinvertebrate assemblages using partial canonical correspondence analysis (pCCA). Hydrol Earth Syst Sci 7: 221–233
Bernhard, AE, Colbert, D, McManus, J, Field, KG (2005) Microbial community dynamics based on 16S rRNA gene profiles in a pacific northwest estuary and its tributaries. FEMS Microbiol Ecol 52: 115–128
Blum, LK, Roberts, MS, Garland, JL, Mills, AL (2004) Distribution of microbial communities associated with the dominant high marsh plants and sediments of the United States east coast. Microb Ecol 48: 375–388
Bossio, DA, Scow, KM (1998) Impacts of carbon and flooding on soil microbial communities: phospholipid fatty acid profiles and substrate utilization patterns. Microb Ecol 35: 265–278
Buchan, A, Newell, SY, Butler, M, Biers, EJ, Hollibaugh, JT, Moran, MA (2003) Dynamics of bacterial and fungal communities on decaying salt marsh grass. Appl Environ Microbiol 69: 6676–6687
Burke, DJ, Hamerlynck, EP, Hahn, D (2002) Interactions among plant species and microorganisms in salt marsh sediments. Appl Environ Microbiol 68: 1157–1164
Chander, K, Brookes, PC (1991) Plant inputs of carbon to metal-contaminated soil and effects on the soil microbial biomass. Soil Biol Biochem 23: 1169
Cushman, SA, Wallin, DO (2002) Separating the effects of environmental, spatial and disturbance factors on forest community structure in the Russian Far East. For Ecol Manag 168: 201–215
Davis, C, Nichols, P (2004) Hydrological Investigation of Concrete Flood Control Channel at UC Berkeley's Richmond Field Station. Water Resource Center Archives, Hydrology. eScholarship Repository, University of California
Denaro, R, D'Auria, G, Di Marco, G, Genovese, M, Troussellier, M, Yakimov, MM, Giuliano, L (2005) Assessing terminal restriction fragment length polymorphism suitability for the description of bacterial community structure and dynamics in hydrocarbon-polluted marine environments. Environ Microbiol 7: 78–87
Dunbar, J, Ticknor, LO, Kuske, CR (2000) Assessment of microbial diversity in four southwestern United States soils by 16S rRNA gene terminal restriction fragment analysis. Appl Environ Microbiol 66: 2943–2950
Dunbar, J, Ticknor, LO, Kuske, CR (2001) Phylogenetic specificity and reproducibility and new method for analysis of terminal restriction fragment profiles of 16S rRNA genes from bacterial communities. Appl Environ Microbiol 67: 190–197
Ellis, RJ, Best, JG, Fry, JC, Morgan, P, Neish, B, Trett, MW, Weightman, AJ (2002) Similarity of microbial and meiofaunal community analyses for mapping ecological effects of heavy-metal contamination in soil. FEMS Microbiol Ecol 40: 113–122
Fan, TWM, Lane, AN, Higashi, RM (2004) An electrophoretic profiling method for thiol-rich phytochelatins and metallothioneins. Phytochem Anal 15: 175–183
Fan, TWM, Lane, AN, Shenker, M, Bartley, JP, Crowley, D, Higashi, RM (2001) Comprehensive chemical profiling of gramineous plant root exudates using high-resolution NMR and MS. Phytochemistry 57: 209–221
Farrelly, V, Rainey, FA, Stackebrandt, E (1995) Effect of genome size and rrn gene copy number on PCR amplification of 16S rRNA genes from a mixture of bacterial species. Appl Environ Microbiol 61: 2798–2801
Federle, TW, Hullar, MA, Livingston, RJ, Meeter, DA, White, DC (1983) Spatial distribution of biochemical parameters indicating biomass and community composition of microbial assemblies in estuarine mud flat sediments. Appl Environ Microbiol 45: 58–63
Ferreira, MT, Rodríguez-González, PM, Aguiar, FC, Albuquerque, A (2005) Assessing biotic integrity in Iberian rivers: development of a multimetric plant index. Ecol Indic 5: 137–149
Findlay, RH, Trexler, MB, White, DC (1990) Response of a benthic microbial community to biotic disturbance. Mar Ecol Prog Ser 62: 135–148
Findlay, RH, Watling, L (1997) Seasonal variation in sedimentary microbial community structure as a backdrop for the detection of anthropogenic stress. In: Eganhouse, RP (Ed.) Molecular Markers in Environmental Geochemistry, American Chemical Society, Washington, DC, pp 49–64
Franklin, RB, Blum, LK, McComb, AC, Mills, AL (2002) A geostatistical analysis of small-scale spatial variability in bacterial abundance and community structure in salt marsh creek bank sediments. FEMS Microbiol Ecol 42: 71–80
Franklin, RB, Mills, AL (2003) Multi-scale variation in spatial heterogeneity for microbial community structure in an eastern Virginia agricultural field. FEMS Microbiol Ecol 44: 335–346
Frostegard, A, Tunlid, A, Baath, E (1993) Phospholipid fatty acid composition, biomass, and activity of microbial communities from two soil types experimentally exposed to different heavy metals. Appl Environ Microbiol 59: 3605–3617
Frostegard, A, Tunlid, A, Baath, E (1996) Changes in microbial community structure during long-term incubation in two soils experimentally contaminated with metals. Soil Biol Biochem 28: 55–63
Giller, KE, Witter, E, McGrath, SP (1998) Toxicity of heavy metals to microorganisms and microbial processes in agricultural soils: a review. Soil Biol Biochem 30: 1389–1414
Hall, JL (2002) Cellular mechanisms for heavy metal detoxification and tolerance. J Exp Bot 53: 1–11
Howes, BL, Weiskel, PK, Geohringer, DD, Teal, JM (1996) Interception of freshwater and nitrogen transport from uplands to coastal waters: the role of salt marshes. In: Nordstrom, KF, Roman, CT (Eds.) Estuarine Shores: Evolution, Environments and Human Alterations, John Wiley & sons, New York, NY, USA, pp 287–310
Hyun, JH, Choi, JK, Chung, KH, Yang, EJ, Kim, MK (1999) Tidally induced changes in bacterial growth and viability in the Macrotidal Han River Estuary, Yellow Sea. Estuar Coast Shelf Sci 48: 143–153
Kang, S, Mills, AL (2004) Soil bacterial community structure changes following disturbance of the overlying plant community. Soil Sci 169: 55–65
Keith-Roach, MJ, Bryan, ND, Bardgett, RD, Livens, FR (2002) Seasonal changes in the microbial community of a salt marsh, measured by phospholipid fatty acid analysis. Biogeochemistry 60: 77–96
Kozdroj, J, van Elsas, JD (2000) Response of the bacterial community to root exudates in soil polluted with heavy metals assessed by molecular and cultural approaches. Soil Biol Biochem 32: 1405–1417
Kozdroj, J, van Elsas, JD (2001) Structural diversity of microorganisms in chemically perturbed soil assessed by molecular and cytochemical approaches. J Microbiol Methods 43: 197–212
Kraufmann, K, Christophersen, M, Buttler, A, Harms, H, Höhener, P (2004) Microbial community response to petroleum hydrocarbon contamination in the unsaturated zone at the experimental field site Værløse, Denmark. FEMS Microbiol Ecol 48: 387–399
Labaune, C, Magnin, F (2001) Land snail communities in Mediterranean upland grasslands: The relative importance of four sets of environmental and spatial variables. J Molluscan Stud 67: 463–474
LaMontagne, MG, Holden, PA (2003) Comparison of free-living and particle-associated bacterial communities in a coastal lagoon. Microb Ecol 46: 228–237
LaMontagne, MG, Michel, FC, Holden, PA, Reddy, CA (2002) Evaluation of extraction and purification methods for obtaining PCR-amplifiable DNA from compost for microbial community analysis. J Microbiol Methods 49: 255–264
LaMontagne, MG, Schimel, JP, Holden, PA (2003) Comparison of subsurface and surface soil bacterial communities in California grassland as assessed by terminal restriction fragment length polymorphisms of PCR-amplified 16S rRNA genes. Microb Ecol 46: 216–227
Lee, BD, Schaller, KD, Watwood, ME, Apel, WA (2000) Transition metal catalyst-assisted reductive dechlorination of perchloroethylene by anaerobic aquifer enrichments. Bioremediat J 4: 97–110
Liu, W-T, Marsh, TL, Cheng, H, Forney, LJ (1997) Characterization of microbial diversity by determining terminal restriction fragment length polymorphisms of genes encoding 16S rRNA. Appl Environ Microbiol 63: 4516–4522
Loffhagen, N, Härtig, C, Babel, W (2004) Pseudomonas putida NCTC 10936 balances membrane fluidity in response to physical and chemical stress by changing the saturation degree and the trans/cis ratio of fatty acids. Biosci Biotechnol Biochem 68: 317–323
Lovell, CR, Bagwell, CE, Czako, M, Marton, L, Piceno, YM, Ringelberg, DB (2001) Stability of a rhizosphere microbial community exposed to natural and manipulated environmental variability. FEMS Microbiol Ecol 38: 69–76
Lowe, M, Madsen, EL, Schindler, K, Smith, C, Emrich, S, Robb, F, Halden, RU (2002) Geochemistry and microbial diversity of a trichloroethene-contaminated Superfund site undergoing intrinsic in situ reductive dechlorination. FEMS Microbiol Ecol 40: 123
Lueders, T, Friedrich, MW (2003) Evaluation of PCR amplification bias by terminal restriction fragment length polymorphism analysis of small-subunit rRNA and mcrA genes by using defined template mixtures of methanogenic pure cultures and soil DNA extracts. Appl Environ Microbiol 69: 320–326
Malinsky, J (2002) UC Ordered to Help in Cleanup of Polluted Stege Marsh in Richmond. The Daily Californian, Berkeley, CA
McCaig, AE, Glover, LA, Prosser, JI (2001) Numerical analysis of grassland bacterial community structure under different land management regimens by using 16S ribosomal DNA sequence data and denaturing gradient gel electrophoresis banding patterns. Appl Environ Microbiol 67: 4554–4559
Moffett, BF, Nicholson, FA, Uwakwe, NC, Chambers, BJ, Harris, JA, Hill, TCJ (2003) Zinc contamination decreases the bacterial diversity of agricultural soil. FEMS Microbiol Ecol 43: 13–19
Muller, AK, Westergaard, K, Christensen, S, Sorensen, SJ (2001) The effect of long-term mercury pollution on the soil microbial community. FEMS Microbiol Ecol 36: 11–19
Niemi, G, Wardrop, D, Brooks, R, Anderson, S, Brady, V, Paerl, H, Rakocinski, C, Brouwer, M, Levinson, B, McDonald, M (2004) Rationale for a new generation of indicators for coastal waters. Environ Health Perspect 112: 979–986
NRC (1994) Priorities for Coastal Ecosystem Science. National Academy of Science, Washington, DC
Nubel, U, Garcia-Pichel, F, Myuzer, G (1977) PCR primers to amplify 16S rRNA from cyanobacteria. Appl Environ Microbiol 63: 3327–3332
O'Leary, WM, Wilkinson, SG (1988) Gram positive bacteria. In: Ratledge, C, Wilkinson, SG (Eds.) Microbial Lipids, Academic Press, London, UK, pp 107–201
Osborn, AM, Moore, ERB, Timmis, KN (2000) An evaluation of terminal-restriction fragment length polymorphism (T-RFLP) analysis for the study of microbial community structure and dynamics. Environ Microbiol 2: 39–50
Page, HM (1996) Fate of Fertilizer-derived Nitrogen Entering a Salt Marsh in Ground Water: Clues from Stable Nitrogen Isotope Ratio Analysis, Southern California Academy of Sciences, California State University, Fullerton, CA, p 58
Page, HM, Petty, RL, Meade, DE (1995) Influence of watershed runoff on nutrient dynamics in a southern California salt marsh. Estuar Coast Shelf Sci 41: 163–180
Palmer, MW. Ordination methods for ecologists. Online website. http://ordination.okstate.edu/
Palmer, MW (1993) Putting things in even better order: the advantages of canonical correspondence analysis. Ecology 74: 2215–2230
Pennanen, T, Frostegard, A, Fritze, H, Baath, E (1996) Phospholipid fatty acid composition and heavy metal tolerance of soil microbial communities along two heavy metal-polluted gradients in coniferous forests. Appl Environ Microbiol 62: 420–428
Perkiomaki, J, Tom-Petersen, A, Nybroe, O, Fritze, H (2003) Boreal forest microbial community after long-term field exposure to acid and metal pollution and its potential remediation by using wood ash. Soil Biol Biochem 35: 1517–1526
Pillai, MC, Vines, CA, Wikramanayake, AH, Cherr, GN (2003) Polycyclic aromatic hydrocarbons disrupt axial development in sea urchin embryos through a beta-catenin dependent pathway. Toxicology 186: 93–108
Pinel-Alloul, B, Methot, G, Lapierre, L, Willsie, A (1996) Macroinvertebrate community as a biological indicator of ecological and toxicological factors in Lake Saint-Francois (Quebec). Environ Pollut 91: 65–87
Polz, MF, Cavanaugh, CM (1998) Bias in template-to-product ratios in multitemplate PCR. Appl Environ Microbiol 64: 3724–3730
Posthuma, L (1997) Effects of toxicants on population and community parameters in field conditions, and their potential use in the validation of risk assessment methods. In: Van Straalen, NM, Løkke, H (Eds.) Ecological Risk Assessment of Contaminants in Soil, Chapman & Hall, London, pp 85–117
Powell, SM, Bowman, JP, Snape, I, Stark, JS (2003) Microbial community variation in pristine and polluted nearshore Antarctic sediments. FEMS Microbiol Ecol 45: 135–145
Ranjard, L, Nazaret, S, Gourbiere, F, Thioulouse, J, Linet, P, Richaume, A (2000) A soil microscale study to reveal the heterogeneity of Hg(II) impact on indigenous bacteria by quantification of adapted phenotypes and analysis of community DNA fingerprints. FEMS Microbiol Ecol 31: 107–115
Ranjard, L, Poly, F, Nazaret, S (2000) Monitoring complex bacterial communities using culture-independent molecular techniques: application to soil environment. Res Microbiol 151: 167–177
Ravit, B, Ehrenfeld, JG, Häggblom, MM (2005) Salt marsh rhizosphere affects microbial biotransformation of the widespread halogenated contaminant tetrabromobisphenol-A (TBBPA). Soil Biol Biochem 37: 1049–1057
Rejmankova, E, Higashi, RM, Roberts, DR, Lege, M, Andre, RG (2001) The use of solid phase microextraction (SPME) devices in analysis for potential mosquito oviposition attractant chemicals from cyanobacterial mats. Aquat Ecol 34: 413–420
Reysenbach, A-L, Giver, LJ, Wickham, GS, Pace, NR (1992) Differential amplification of rRNA genes by polymerase chain reaction. Appl Environ Microbiol 58: 3417–3418
Rondon, MR, Goodman, RM, Handelsman, J (1999) The earth's bounty: assessing and accessing soil microbial diversity. Trends Biotechnol 17: 403–409
Skorupa, JP (1998) Selenium poisoning of fish and wildlife in nature: lessons from twelve realworld examples. In: Frankenberger, WT, Engberg, RA (Eds.) Environmental Chemistry of Selenium, Marcel Dekker, Inc, New York, pp 315–354
Slack, JMW (1991) From Egg to Embryo: Regional Specification in Early Development. Cambridge University Press, New York, pp 112–115
Smith, SV, Hollibaugh, JT (1993) Coastal metabolism and the oceanic organic-carbon balance. Rev Geophys 31: 75–89
Stolz, JF, Oremland, RS (1999) Bacterial respiration of arsenic and selenium. FEMS Microbiol Rev 23: 615–627
Suhadolc, M, Schroll, R, Gattinger, A, Schloter, M, Munch, JC, Lestan, D (2004) Effects of modified Pb-, Zn-, and Cd-availability on the microbial communities and on the degradation of isoproturon in a heavy metal contaminated soil. Soil Biol Biochem 36: 1943–1954
Suzuki, M, Rappe, MS, Giovannoni, SJ (1998) Kinetic bias in estimates of coastal picoplankton community structure obtained by measurements of small-subunit rRNA gene PCR amplicon length heterogeneity. Appl Environ Microbiol 64: 4522–4529
Suzuki, MT, Giovannoni, SJ (1996) Bias caused by template annealing in the amplification of mixtures of 16S rRNA genes by PCR. Appl Environ Microbiol 62: 625–630
Teal, JM, Howes, BL (2000) Salt marsh values: retrospection from the end of the century. In: Weinstain, MP, Kreeger, DA (Eds.) Concepts and Controversies in Tidal Marsh Ecology, Kluwer Academic Publishers, Dordrecht, The Netherlands, pp 3–7
ter Braak, CJF (1986) Canonical correspondence analysis: a new eigenvector technique from multivariate direct gradient analysis. Ecology 67: 1167–1179
ter Braak, CJF (1987) The analysis of vegetation–environment relationships by canonical correspondence analysis. Vegetatio 69: 69–77
ter Braak, CJF (1995) Ordination. In: Jongman, RHG, ter Braak, CJF, van Tongeren, OFR (Eds.) Data Analysis in Community and Landscape Ecology, Cambridge University Press, New York, pp 91–173
ter Braak, CJF, Smilauer, P (2002) CANOCO Reference Manual and CanoDraw for Windows User's Guide: Software for Canonical Community Ordination (version 4.5). Microcomputer Power, Ithaca, NY, USA, 500 p
Turpeinen, R, Kairesalo, T, Haggblom, MM (2004) Microbial community structure and activity in arsenic-, chromium- and copper-contaminated soils. FEMS Microbiol Ecol 47: 39–50
U.S. EPA (1994) Method 6020, Inductively coupled plasma–mass spectrometry. In publication SW-846, Test Methods for Evaluating Solid Waste, Physical/Chemical Methods, EPA Office of Solid Waste, Washington, DC
U.S. EPA (2002) Test Method 1008.0-sea urchin, Arbacia punctulata, fertilization. In EPA-821-R-02-014, Short-term Methods for Estimating the Chronic Toxicity of Effluents and Receiving Waters to Marine and Estuarine Organisms, EPA Office of Water, Washington, DC
Greiner, WC (1999) University of California, Berkeley Richmond Field Station Field Sampling and Analysis Plan and Tiered Rish Evaluation, Unpublished Report from the University of California, Berkeley, URS. Oakland, CA
Venables, WN, Ripley, BD (2002) Modern Applied Statistics with S, 4th ed. Springer-Verlag, New York, p 512
Vestal, JR, White, DC (1989) Lipid analysis in microbial ecology: quantitative approaches to the study of microbial communities. BioScience 39: 535–541
White, DC, Flemming, CA, Leung, KT, Macnaughton, SJ (1998) In situ microbial ecology for quantitative appraisal, monitoring, and risk assessment of pollution remediation in soils, the subsurface, the rhizosphere and in biofilms. J Microbiol Methods 32: 93–105
White, DC, Pinkart, HC, Ringelberg, DB (1997) Biomass measurements: biochemical approaches. In: Hurst, CJ, Knudsen, GR, McInerney, MJ, Stetzenbach, LD, Walter, MV (Eds.) Manual of Environmental Microbiology, ASM Press, Washington, DC, pp 91–101
Wilde, SB, Plante, CJ (2002) Spatial heterogeneity of bacterial assemblages in marine sediments: the influence of deposit feeding by Balanoglossus aurantiacus. Estuar Coast Shelf Sci 55: 97–107
Wintzingerode, FV, Goebel, UB, Stackebrandt, E (1997) Determination of microbial diversity in environmental samples: Pitfalls of PCR-based rRNA analysis. FEMS Microbiol Rev 21: 213–229
Zelles, L (1997) Phospholipid fatty acid profiles in selected members of soil microbial communities. Chemosphere 35: 275–294
Zelles, L (1999) Fatty acid patterns of phospholipids and lipopolysaccharides in the characterisation of microbial communities in soil: a review. Biol Fertil Soils 29: 111–129
Zelles, L, Bai, QY, Rackwitz, R, Chadwick, D, Beese, F (1995) Determination of phospholipid- and lipopolysaccharide-derived fatty acids as an estimate of microbial biomass and community structures in soils. Biol Fertil Soils 19: 115–123
Acknowledgments
This work was performed in part at the University of California Natural Reserve System Carpinteria Salt Marsh Reserve. Funding for this work was provided by U.S. Environmental Protection Agency's STAR Estuarine and Great Lakes (EaGLe) Program through U.S. EPA Agreement #R-88286760, through a Mildred E. Mathias Graduate Student Research Grant from the University of California Natural Reserve System, and by the University of California Toxic Substance Research & Teaching Program (UC TSR&TP). We acknowledge the assistance of William Sprague in data management, Chuanjie Zhou for graphics, Jane Choe for laboratory assistance, Laurie Van De Werfhorst for assisting with TRFLP analysis, and Andy Brooks and Noah Fierer for insightful discussions.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Cao, Y., Cherr, G.N., Córdova-Kreylos, A.L. et al. Relationships between Sediment Microbial Communities and Pollutants in Two California Salt Marshes. Microb Ecol 52, 619–633 (2006). https://doi.org/10.1007/s00248-006-9093-1
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00248-006-9093-1