Wetlands

, Volume 36, Issue 2, pp 361–371 | Cite as

Effects of Salinity and Inundation on Microbial Community Structure and Function in a Mangrove Peat Soil

  • Lisa G. Chambers
  • Rafael Guevara
  • Joseph N. Boyer
  • Tiffany G. Troxler
  • Stephen E. Davis
Original Research

Abstract

Shifts in microbial community function and structure can be indicators of environmental stress and ecosystem change in wetland soils. This study evaluated the effects of increased salinity, increased inundation, and their combination, on soil microbial function (enzyme activity) and structure (phospholipid fatty acid (PLFA) signatures and terminal restriction fragment length polymorphisms (T-RFLP) profiles) in a brackish mangrove peat soil using tidal mesocosms (Everglades, Florida, USA). Increased tidal inundation resulted in reduced soil enzyme activity, especially alkaline phosphatase, an increase in the abundance and diversity of prokaryotes, and a decline in number of eukaryotes. The community composition of less abundant bacteria (T-RFLPs comprising 0.3–1 % of total fluorescence) also shifted as a result of increased inundation under ambient salinity. Several key biogeochemical indicators (oxidation-reduction potential, CO2 flux, porewater NH4+, and dissolved organic carbon) correlated with measured microbial parameters and differed with inundation level. This study indicates microbial function and composition in brackish soil is more strongly impacted by increased inundation than increased salinity. The observed divergence of microbial indicators within a short time span (10-weeks) demonstrates their usefulness as an early warning signal for shifts in coastal wetland ecosystems due to sea level rise stressors.

Keywords

Coastal wetland Peat Sea level rise Salinity Mangrove 

References

  1. Alongi DM (2008) Mangrove forests: resilience, protection from tsunamis, and responses to global climate change. Estuar Coast Shelf Sci 76:1–13. doi:10.1016/j.ecss.2007.08.024 CrossRefGoogle Scholar
  2. Bell CW, Fricks BE, Rocca JD, et al (2013) High-throughput fluorometric measurement of potential soil extracellular enzyme activities. J Visualized Exp: JoVE e50961. doi:10.3791/50961
  3. Berner EK, Berner RA (2012) Global environment: Water, air, and geochemical cycles. Princeton University Press, Princeton, NYGoogle Scholar
  4. Billings SA, Ziegler SE (2008) Altered patterns of soil carbon substrate usage and heterotrophic respiration in a pine forest with elevated CO2 and N fertilization. Glob Chang Biol 14:1025–1036. doi:10.1111/j.1365-2486.2008.01562.x CrossRefGoogle Scholar
  5. 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. doi:10.1007/s002489900082 CrossRefPubMedGoogle Scholar
  6. Bouvier TC, del Giorgio PA (2002) Compositional changes in free-living bacterial communities along a salinity gradient in two temperate estuaries. Limnol Oceanogr 47:453–470CrossRefGoogle Scholar
  7. Boyer JN, Fourqurean JW, Jones RD (1997) Spatial characterization of water quality in Florida Bay and Whitewater Bay by multivariate analyses: zones of similar influence. Estuaries 20:743. doi:10.2307/1352248 CrossRefGoogle Scholar
  8. Capone DG, Kiene RP (1988) Comparison of microbial dynamics in marine and Freshwater sediments: contrasts in anaerobic carbon catabolism. Limnol Oceanogr 33:725–749CrossRefGoogle Scholar
  9. Casamayor EO, Massana R, Benlloch S, et al. (2002) Changes in archaeal, bacterial and eukaryal assemblages along a salinity gradient by comparison of genetic fingerprinting methods in a multipond solar saltern. Environ Microbiol 4:338–348. doi:10.1046/j.1462-2920.2002.00297.x CrossRefPubMedGoogle Scholar
  10. Chambers LG, Davis SE, Troxler TG, et al. (2014) Biogeochemical effects of simulated sea level rise on carbon loss in an Everglades mangrove peat soil. Hydrobiologia 726:195–211. doi:10.1007/s10750-013-1764-6 CrossRefGoogle Scholar
  11. Chambers LG, Davis SE, Troxler TG (2015) Sea level rise in the Everglades: plant-soil-microbial feedbacks in response to changing physical conditions. In: Entry JA, Gottlieb AD, Jayachandrahan K, Ogram A (eds) Microbiology of the Everglades ecosystem. CRC Press, Boca Raton, pp. 89–112Google Scholar
  12. Chambers LG, Osborne TZ, Reddy KR (2013) Effect of salinity-altering pulsing events on soil organic carbon loss along an intertidal wetland gradient: a laboratory experiment. Biogeochemistry 115:363–383. doi:10.1007/s10533-013-9841-5 CrossRefGoogle Scholar
  13. Chambers LG, Reddy KR, Osborne TZ (2011) Short-term response of carbon cycling to salinity pulses in a Freshwater Wetland. Soil Sci Soc Am J 75:2000–2007. doi:10.2136/sssaj2011.0026 CrossRefGoogle Scholar
  14. Chrost RJ, Krambeck HJ (1986) Fluorescence correction for measurements of enzyme-activity in natural-waters using methylumbelliferyl substrates. Archiv Fur Hydrobiologie 106:79–90Google Scholar
  15. Chrost RJ, Overbeck J (1987) Kinetics of alkaline-phosphatase activity and phosphorus availability for phytoplankton and bacterioplankton in Lake Plusssee (North-German eutrophic lake). Microb Ecol 13:229–248. doi:10.1007/bf02025000 CrossRefPubMedGoogle Scholar
  16. Córdova-kreylos AL, Cao Y, Green PG, et al. (2006) Diversity, composition, and geographical distribution of microbial communities in California Salt Marsh Sediments Diversity, composition, and geographical distribution of microbial communities in California Salt Marsh Sediments. Appl Environ Microbiol 72:3357–3366. doi:10.1128/AEM.72.5.3357 CrossRefPubMedPubMedCentralGoogle Scholar
  17. Davis SM (1991) Growth, decomposition, and nutrient retention of Cladium-jamaicense crantz and Typha-domingensis pres in the Florida Everglades. Aquat Bot 40:203–224CrossRefGoogle Scholar
  18. Day JW, Christian RR, Boesch DM, et al. (2008) Consequences of climate change on the ecogeomorphology of coastal wetlands. Estuar Coasts 31:477–491. doi:10.1007/s12237-008-9047-6 CrossRefGoogle Scholar
  19. Delaune RD, Smith CJ, Patrick WH (1983) Methane release from Gulf-coast wetlands. Tellus Ser B Chem Phys Meteorol 35:8–15CrossRefGoogle Scholar
  20. Donnelly JP, Bertness MD (2001) Rapid shoreward encroachment of salt marsh cordgrass in response to accelerated sea-level rise. Proc Natl Acad Sci U S A 98:14218–14223. doi:10.1073/pnas.251209298 CrossRefPubMedPubMedCentralGoogle Scholar
  21. 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 67:190–197CrossRefPubMedPubMedCentralGoogle Scholar
  22. Fagherazzi S, Kirwan ML, Mudd SM, et al (2012) Numerical models of salt marsh evolution: ecological, geomorphic, and climate factors. Rev Geophys 50:28. doi:10.1029/2011rg000359
  23. Frankenberger WT, Bingham JFT (1982) Influence of salinity on Soil enzyme activities. Soil Sci Soc Am J 46:1173–1177CrossRefGoogle Scholar
  24. Frostegård Å, Bååth E, Tunlio A (1993) Shifts in the structure of soil microbial communities in limed forests as revealed by phospholipid fatty acid analysis. Soil Biol Biochem 25:723–730. doi:10.1016/0038-0717(93)90113-P CrossRefGoogle Scholar
  25. Gedan KB, Kirwan ML, Wolanski E, et al. (2011) The present and future role of coastal wetland vegetation in protecting shorelines: answering recent challenges to the paradigm. Clim Chang 106:7–29. doi:10.1007/s10584-010-0003-7 CrossRefGoogle Scholar
  26. Gedan KB, Silliman BR, Bertness MD (2009) Centuries of human-driven change in Salt Marsh Ecosystems. Ann Rev Mar Sci 1:117–141. doi:10.1146/annurev.marine.010908.163930 CrossRefPubMedGoogle Scholar
  27. Gribsholt B, Kristensen E (2003) Benthic metabolism and sulfur cycling along an inundation gradient in a tidal Spartina anglica salt marsh. Limnol Oceanogr 48:2151–2162CrossRefGoogle Scholar
  28. Hopfensperger KN, Burgin AJ, Schoepfer VA, Helton AM (2014) Impacts of saltwater incursion on plant communities, anaerobic microbial metabolism, and resulting relationships in a restored Freshwater wetland. Ecosystems 17:792–807. doi:10.1007/s10021-014-9760-x CrossRefGoogle Scholar
  29. Hoppe H-G (1993) Use of fluorogenic model substrates for extracellular enzyme activity (EEA) measurement of bacteria. Handbook of methods in aquatic microbial ecology 423–431Google Scholar
  30. Howarth W (1984) The ecological significance of sulfur in the energy dynamics of salt marsh and coastal marine sediments. Biogeochemistry 1:5–27CrossRefGoogle Scholar
  31. Ikenaga M, Guevara R, Dean AL, et al. (2010) Changes in community structure of sediment bacteria along the Florida Coastal Everglades Marsh-Mangrove-Seagrass salinity gradient. Microb Ecol 59:284–295. doi:10.1007/s00248-009-9572-2 CrossRefPubMedGoogle Scholar
  32. Inglett KS, Inglett PW, Reddy KR (2011) Soil Microbial Community composition in a restored calcareous subtropical Wetland. Soil Sci Soc Am J 75:1731–1740. doi:10.2136/sssaj2010.0424 CrossRefGoogle Scholar
  33. Jackson CR, Vallaire SC (2009) Effects of salinity and nutrients on microbial assemblages in Louisiana wetland sediments. Wetlands 29:277–287CrossRefGoogle Scholar
  34. Jin XB, Huang JY, Zhou YK (2012) Impact of coastal wetland cultivation on microbial biomass, ammonia-oxidizing bacteria, gross N transformation and N2O and NO potential production. Biol Fertil Soils 48:363–369. doi:10.1007/s00374-011-0631-8 CrossRefGoogle Scholar
  35. Josephson KL, Gerba CP, Pepper IL (1993) Polymerase chain-reaction detection of nonviable bacterial pathogens. Appl Environ Microbiol 59:3513–3515PubMedPubMedCentralGoogle Scholar
  36. McKee KL (1993) Soil physicochemical patterns and mangrove species distribution–reciprocal effects? J Ecol 81:477. doi:10.2307/2261526 CrossRefGoogle Scholar
  37. Mentzer JL, Goodman RM, Balser TC (2006) Microbial response over time to hydrologic and fertilization treatments in a simulated wet prairie. Plant Soil 284:85–100. doi:10.1007/s11104-006-0032-1 CrossRefGoogle Scholar
  38. Morris JT, Sundareshwar PV, Nietch CT, et al. (2002) Responses of coastal wetlands to rising sea level. Ecology 83:2869–2877CrossRefGoogle Scholar
  39. Morrissey EM, Berrier DJ, Neubauer SC, Franklin RB (2014a) Using microbial communities and extracellular enzymes to link soil organic matter characteristics to greenhouse gas production in a tidal freshwater wetland. Biogeochemistry 117:473–490. doi:10.1007/s10533-013-9894-5 CrossRefGoogle Scholar
  40. Morrissey EM, Gillespie JL, Morina JC, Franklin RB (2014b) Salinity affects microbial activity and soil organic matter content in tidal wetlands. Glob Chang Biol 20:1351–1362. doi:10.1111/gcb.12431 CrossRefPubMedGoogle Scholar
  41. Nannipieri P, Ascher J, Ceccherini MT, et al. (2003) Microbial diversity and soil functions. Eur J Soil Sci 54:655–670. doi:10.1046/j.1351-0754.2003.0556.x CrossRefGoogle Scholar
  42. Neubauer SC (2011) Ecosystem responses of a tidal Freshwater Marsh Experiencing Saltwater intrusion and altered hydrology. Estuar Coasts 36:491–507. doi:10.1007/s12237-011-9455-x CrossRefGoogle Scholar
  43. Neumann JE, Yohe G, Nicholls RJ, Manion M (2000) Sea-level rise & global climate change: a review of impacts to U.S. coasts. 1–43Google Scholar
  44. Nicholls RJ, Hoozemans FMJ, Marchand M (1999) Increasing flood risk and wetland losses due to global sea-level rise: regional and global analyses. Glob Environ Chang Hum Pol Dimens 9:S69–S87CrossRefGoogle Scholar
  45. Portnoy JW, Giblin AE (1997) Biogeochemical effects of seawater restoration to diked salt marshes. Ecol Appl 7:1054–1063. doi:10.1890/1051-0761(1997)007[1054:beosrt]2.0.co;2 CrossRefGoogle Scholar
  46. Rietz DN, Haynes RJ (2003) Effects of irrigation-induced salinity and sodicity on soil microbial activity. Soil Biol Biochem 35:845–854. doi:10.1016/s0038-0717(03)00125-1 CrossRefGoogle Scholar
  47. Rivera-Monroy VH, de Mutsert K, Twilley RR, et al. (2007) Patterns of nutrient exchange in a riverine mangrove forest in the Shark River Estuary, Florida, USA. Hydrobiologia 17:169–178Google Scholar
  48. Ross MS, Meeder JF, Sah JP, et al. (2000) The Southeast Saline Everglades revisited: 50 years of coastal vegetation change. J Veg Sci 11:101–112. doi:10.2307/3236781 CrossRefGoogle Scholar
  49. Shade A, Jones SE, Caporaso JG, et al. (2014) Conditionally rare taxa disproportionately contribute to temporal changes in microbial diversity. mBio 5:e01371–e01314. doi:10.1128/mBio.01371-14 CrossRefPubMedPubMedCentralGoogle Scholar
  50. Sherman RE, Fahey TJ, Howarth RW (1998) Forest: in a neotropical interactions mangrove and sulfur dynamics iron, phosphorus. Oecologia 115:553–563. doi:10.1007/s004420050553 CrossRefGoogle Scholar
  51. Sinsabaugh RL (1994) Enzymatic analysis of microbial pattern and process. Biol Fertil Soils 17:69–74. doi:10.1007/bf00418675 CrossRefGoogle Scholar
  52. Smith TJ, Anderson GH, Balentine K, et al. (2009) Cumulative impacts of hurricanes on Florida mangrove ecosystems: sediment deposition, storm surges and vegetation. Wetlands 29:24–34. doi:10.1672/08-40.1 CrossRefGoogle Scholar
  53. Sparling GP (1992) Ratio of microbial biomass carbon to soil organic-carbon as a sensitive indicator of changes in soil organic-matter. Aust J Soil Res 30:195–207. doi:10.1071/sr9920195 CrossRefGoogle Scholar
  54. Sparling GP, Feltham CW, Reynolds J, et al. (1990) Estimation of soil microbial c by a fumigation-extraction method: use on soils of high organic matter content, and a reassessment of the kec-factor. Soil Biol Biochem 22:301–307. doi:10.1016/0038-0717(90)90104-8 CrossRefGoogle Scholar
  55. Teh SY, DeAngelis DL, Sternberg LDSL, et al. (2008) A simulation model for projecting changes in salinity concentrations and species dominance in the coastal margin habitats of the Everglades. Ecol Model 213:245–256. doi:10.1016/j.ecolmodel.2007.12.007 CrossRefGoogle Scholar
  56. Titus JG, Richman C (2001) Maps of lands vulnerable to sea level rise: modeled elevations along the US Atlantic and Gulf coasts. Clim Res 18:205–228CrossRefGoogle Scholar
  57. Troxler TG, Ikenaga M, Scinto L, et al. (2012) Patterns of Soil bacteria and Canopy Community structure related to tropical peatland development. Wetlands 32:769–782. doi:10.1007/s13157-012-0310-z CrossRefGoogle Scholar
  58. Unger IM, Kennedy AC, Muzika RM (2009) Flooding effects on soil microbial communities. Appl Soil Ecol 42:1–8. doi:10.1016/j.apsoil.2009.01.007 CrossRefGoogle Scholar
  59. Van Ryckegem G, Verbeken A (2005) Fungal diversity and community structure on Phragmites australis (Poaceae) along a salinity gradient in the Scheldt estuary (Belgium). Nova Hedwigia 80:173–197. doi:10.1127/0029-5035/2005/0080-0173 CrossRefGoogle Scholar
  60. Vance ED, Brookes PC, Jenkinson DS (1987) An extraction method for measuring soil microbial biomass-C. Soil Biol Biochem 19:703–707CrossRefGoogle Scholar
  61. Vestal JR, White DC (1989) Lipid analysis in microbial ecology- quantitative approaches to the study of microbial communties. Bioscience 39:535–541. doi:10.2307/1310976 CrossRefPubMedGoogle Scholar
  62. Welch R, Madden M, Doren RF (1999) Mapping the Everglades. Photogramm Eng Remote Sens 65:163–170Google Scholar
  63. Weston NB, Dixon RE, Joye SB (2006) Ramifications of increased salinity in tidal freshwater sediments: geochemistry and microbial pathways of organic matter mineralization. J Geophys Res Biogeosci 111:14. doi:10.1029/2005jg000071 Google Scholar
  64. Weston NB, Vile MA, Neubauer SC, Velinsky DJ (2011) Accelerated microbial organic matter mineralization following salt-water intrusion into tidal freshwater marsh soils. Biogeochemistry 102:135–151. doi:10.1007/s10533-010-9427-4 CrossRefGoogle Scholar
  65. White JR, Reddy KR (2001) Influence of selected inorganic electron acceptors on organic nitrogen mineralization in everglades soils. Soil Sci Soc Am J 65:941–948CrossRefGoogle Scholar
  66. Williams K, Ewel KC, Stumpf RP, et al. (1999) Sea-level rise and coastal forest retreat on the west coast of Florida, USA. Ecology 80:2045–2063CrossRefGoogle Scholar
  67. Wright AL, Reddy KR (2001) Phosphorus loading effects on extracellular enzyme activity in everglades wetland soils. Soil Sci Soc Am J 65:588–595CrossRefGoogle Scholar
  68. Ye RZ, Jin QS, Bohannan B, et al. (2014) Homoacetogenesis: A potentially underappreciated carbon pathway in peatlands. Soil Biol Biochem 68:385–391. doi:10.1016/j.soilbio.2013.10.020 CrossRefGoogle Scholar
  69. Zogg GP, Zak DR, Ringelberg DB, et al. (1997) Compositional and functional shifts in microbial communities due to soil warming. Soil Sci Soc Am J 61:475–481CrossRefGoogle Scholar

Copyright information

© Society of Wetland Scientists 2016

Authors and Affiliations

  • Lisa G. Chambers
    • 1
  • Rafael Guevara
    • 2
  • Joseph N. Boyer
    • 3
  • Tiffany G. Troxler
    • 4
  • Stephen E. Davis
    • 5
  1. 1.Department of BiologyUniversity of Central FloridaOrlandoUSA
  2. 2.Biocollections Worldwide, Inc.MiamiUSA
  3. 3.Center for the EnvironmentPlymouth State UniversityPlymouthUSA
  4. 4.Southeast Environmental Research CenterFlorida International UniversityMiamiUSA
  5. 5.Everglades FoundationPalmetto BayUSA

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