- 1 Introduction
- 2 Physical environment
- 3 Biological interactions
- 4 Microbial processes
- 5 Key Microorganisms
- 6 Current Research
- 7 References
Salt marshes represent a transitional zone between terrestrial and marine ecosystems resulting in one of the most biologically productive habitats on earth. This productivity plays a major role in the nutrient cycles and food webs for both terrestrial as well as marine ecosystems. Migratory birds find abundant food resources from insects, mollusks, arthropods and fish. Marine fauna utilize the nutrient rich habitat establishing critical reproductive sites for invertebrates and vertebrates groups including oysters, crabs, sharks and other fish species. This productivity is a result of major conflicting environmental factors that create harsh conditions with stressful levels of salinity, water submergence and low oxygen levels. Environmental conditions are shaped by daily tidal surges, major changes in seasonal fluctuations of freshwater, saltwater inundation during the occasional storm surges, and increased salinity during seasonal dry periods and evapotranspiration. Salinity at or greater than sea water at 34 g l-1 (3.4%) is the norm throughout the salt marsh resulting in significant Na fluxes. Regular inundation with fresh and salt water creates dramatic fluctuations in soil oxygen levels and sediment deposits. These extremes in salt and water saturations are beyond the tolerance of all but a few highly specialized organisms. Accumulated plant biomass and terrestrial runoff creates an exceptional N cycle. Essential to the productivity of the salt marsh through these various nutrient and chemical fluctuations is a diverse and unique microbial community supporting the flora and fauna of this habitat and sustaining the associated marine environment.
Salt marshes are influenced by three major environmental variables; salinity gradients, reoccurring water table changes and anaerobic conditions associated with saturated soils. Salt from marine water is the dominant factor in salt marsh habitats. While sea water salinity (3.4%) is found throughout the marsh, evapotranspiration results in salinity frequently double sea water. Some soils become hypersaline (>10%) as a result of tidal flooding trapping water at higher elevations allowing evapotranspiration to concentrate salinity. Mean high water level results in substantial changes in soil salinity and subsequent plant community composition. 7% salinity prevents most salt marsh plant species from becoming established. Monotypic stands of cordgrass (Spartina spp.) develop In many temperate climate salt marshes. Spartina is one of the few plants capable of tolerating and growing in the higher saline environment. (Zedler, 2008)
Microbes are confronted with several environmental barriers. High salinity creates problems of osmotic regulation and disrupts enzyme activity. A thin aerobic sediment layer with abundant organic material is accompanied by periodic submergence. Immediately below the aerobic lay is an extended layer with frequent anaerobic conditions followed by a much deeper layer of continuous saturated soil with low organic matter and high saline conditions. These conditions in association with a monotypic plant community provide limited resources for the microbial community specialized to cope with these conditions.
Salt marshes are typically divided into a high, middle and low marsh zone based on elevation but responding to soil salinity established by tidal occurrence. Neap tides occur when the difference between high and low tide is the least, the lowest level of high tide occurring twice a month during the first and third quarters of the moon. Mean high water level is the average higher high-tide level during lower amplitude neap tides. Halophytic plants are usually able to become established above this mean high water level (Zedler, et al., 2008). The mean higher high water level determines the salinity maximum. The vertical width of the maximum salinity band is determined by tidal irregularities which may lead to formation of salt barrens or flats (Wang, H., 2007).
Soil and Geochemical Profile
Plants will slow water flow thus trapping sediment with roots and rhizomes. This trapped sediment is easily lost at the next water surge unless immobilized. Biofilms (algae, fungi and bacteria) produce mucilage which cements sediment particles to form initial soils. Biofilm of cyanobacteria will also coat plant stems. Floating mats of green macro algae collect sediment and help build additional soils when trapped on higher elevations. Marsh soils have high levels of sulfur from the marine water easily observed as the blacken soil which smells like rotten eggs. Coloration and odor are a result of the microbial formation of sulfide. This higher sulfide is another factor reducing the number of plants capable of growing in this habitat. Soils are often anoxic immediately below the surface due to high organic matter and abundant moisture for microorganisms. Roots and burrowing invertebrate bioturbation create micro pores within the soil which aid in aeration. Bioturbation also causes re-suspended and erosion during tidal activity. Biofilms help counter bioturbation thus inhibiting erosion. (Zedler, et al., 2008)
Wilms, R. et al., (2006) produced a geochemical profile of tidal-flat sediments close to the island of Spiekeroog, Germany. Sulfate concentrations reached 30 mM at the surface. Beneath 50 cm sulfate decreased to concentrations below 1 mM. At 250 cm, a second maximum of pore water sulfate was detected, with concentrations ranging from 5.3 to 11.5 mM. Sulfate was depleted below 400 cm with concentrations below .2 mM. Methane was depleted along the anoxic part of the sediment with concentrations below detection limit at the surface. Highest methane value (125 uM) was measured in the sulfate minimum zone (100 and 200 cm). At the deepest layer (450 cm) 100 uM methane was detected. Maximum ammonium concentrations (4.6 to 8.8 mM) were found within the lower part of the sand-dominated interval and the upper shell layers (120 to 200 cm). Beneath this peak, concentrations did not decrease below 1 mM. TOC in the sand-dominated sediments was generally below 0.5%. Higher values (up to 1.3%) were found only for thin intercalations of black mud. These values indicate several different chemical gradients are occurring simultaneously.
Organic matter is provided by a very limited number of resources. Roots and stems from Spartina provide a thin layer of carbon on the sediment surface. Autotrophs, cyanobacteria and green algae, provide additional useable carbon. Characteristic of the salt marsh is the limited organic matter restricted to the upper few centimeters of sediment. Anoxic conditions slow the decomposition with carbon accumulating as peat (Zedler, 2008). Microbial community immobilizes and mineralizes most of the carbon produced (Kuehn, 2000). While wetland plants contribute to the majority of the primary production, only a small fraction of the produced biomass accumulates in the marsh with the majority relocated to other areas through tidal activity (Sousa, 2010)
Salt marshes are often the recipient of large concentrations of nitrogen because of their small size in relations to the size of the watershed that provides freshwater runoff. Most of the water sourced nitrogen simply passes through the salt marsh and becomes part of the aquatic portion of the nitrogen cycle in the ocean. Nitrogen fixation and atmospheric deposition are major factors in salt marsh soils. Approximately 55% of the nitrogen from land and fixation are exported to the ocean. The remainder is stored or denitrified making salt marshes both sinks and sources of nitrogen. (Hopkinson, 2008)
Phosphorus is not directly limiting to salt marshes but it provides an indirect limitation. Sundareshwar ( 2003 ), has shown that while plants are limited by nitrogen, bacteria that support the plants in marsh habitat are limited by phosphorus. Phosphorus limits inhibit the growth of nitrogen-transforming bacteria which also affect carbon fixation, storage and release by plants. Phosphorus availability has major implications for salt marsh communities.
Most plants are unable to cope with the near surface salt water conditions. In contrast, the microbial community including green algae, cyanobacteria, diatoms and flagellates are diverse in species and functional groups. Some plants adopt unique means for dealing with salt. Turtle weed (Batis maritime) continually drops its older leaves with high salt concentration as a means of salt removal providing organic matter for microbes immediately below the plant and enriching the carbon cycle. In temperate climates cordgrass (Spartina spp) often becomes the lone botanical representative. Near surface water limits the root system depth and subsequently the organic resources needed by microbes at lower depths. At higher elevation where brackish conditions prevail, cattails (Typha spp.) become the dominate species. The more competitive cattail prevails in the less harsh conditions while the more stress tolerant species of cordgrass will dominate the salt marsh providing much needed carbon for the microbial community.(Zedler, 2008)
Salt marshes are limited in the number of animals that utilize this habitat. Fish find a rich nutrient source in the water associated with the marshes but have little impact on the habitat. Predominate fauna inhabitats are birds and invertebrates particularly fiddler crabs. While most birds are migratory using the fish population as a nutrient source they provide a nitrogen source for the microbial community in the form of urea. Fiddler crabs provide a unique function by extending aerobic conditions deeper within the sediment. Burrowing activity increases oxidation within the soil sometimes as deep as 50 cm below the sediment surface. Labile organic matter from plant material is largely restricted to the surface creating a sharp redox gradient with the highest density of aerobic microbes in the upper 10 cm. Roots and crab burrows enhance the limited mixing that occurs in the vertical separation between the aerobic and anaerobic conditions (Koretsky, 2005).
A study of small-scale variations in bacterial abundance and community structure was made of salt marsh sediments from Virginia’s eastern shore. Microbial patch size, amount of spatial autocorrelation among samples and the relative importance of horizontal versus vertical separation of communities was analyzed. Significant autocorrelation was found among samples separated by 25 cm vertically and 115 cm horizontally. Variability was much greater in the vertical distance than horizontal reflecting the influence of different environmental parameters primarily drainage and redox potential. (Franklin, 2002) It is worth noting that this study was conducted in an unvegetated area without benefit of the influence of roots and rhizoshperes. Other studies have found similar distinct spatial as well as temporal trends based on redox stratification and seasonal changes in macrofaunal activity and liable organic matter carbon availability. (Koretsky, 2005)
Wilms, (2006) developed a comprehensive vertical profile of tidal-flat / salt marsh microbial community using domain specific PCR and DGGE. Dominant bacteria were Gammaproteobacteria found almost exclusively in the upper sand-dominated area with Firmicutes, Bacteroidetes, and Chloroflexi detected mainly within the deepest layers at 220 cm and below. Archaeal sequences belonging to Methanosarcinales were found long the entire sediment column. Methanomicrobiales were detected in the upper 180 cm. Sequences affiliated with Methanobacteriales and Thermococcales were found in deeper layers. Ciliophora, Gastrotricha, Euglenozoa, and Platyhelminthes were identified in eukaryotic sequences along with Arthropoda, Nematoda, and the diatom-feeding Phagomyxa. Eukaryotic phylotypes decreased with depth from 10 at the surface to 5 beneath 160 cm. In summary, this study found bacterial communities appeared to be affected mainly by the availability and quality of carbon sources, while archaeal-community composition correlated with methane and sulfate concentrations. Archaea distributions are the result of competition with sulfate-reducing bacteria competing directly for hydrogen. (Wilms, 2006)
Fungi and bacteria are important in the decomposition of salt marsh vegetation. Dean Creek Marsh, Sapelo Island, Ga was studied for composition of fungi and bacteria associated with decomposition of Spartina alterniflora. Four major ascomycete fungal groups were dominate in association with decaying leaf blades. These were identified as Phaeosphaeria spartinicola, Mycosphaerella sp., Phaeosphaeria halima and Buergenerula spartinae. Bacteria were predominately Erythrobacter, Agrobacterium and Roseobacter. (Buchan,A., 2003)
Rhizosphere Soil Bacteria
Organic matter in salt marshes is most often associated with the decomposition of grasses which is restricted to the sediment surface. Another source of high quality C is the rhizosphere and the exudates from roots. A study of bacterial community in association with plant succession along the Yangtze River Estuary provided insight into the association of bacteria to specific plant rhizosphere. Three vegetational zones were identified. Phragmites australis and Scirpus mariqueter were native to the area while an invasive Spartina alterniflora was deliberately introduced. The natural succession of plants is from mudflats to Scirpus which progresses to Phragmites. Low elevations are dominated by Scirpus with higher elevations by Phragmites. The most abundant bacteria were members of Alphaproteobacteria, Betaproteobacteria, Gammaproteobacteria and Deltaproteobacteria. Scirpus (low elevation) had the highest bacterial richness and Phragmites (high elevation) the lowest associated richness. Spartina inhabited the area between the two grass communities and had an intermediate associated richness of bacteria. It was concluded that root exudates of the different plant species influenced the bacterial diversity. No physical and chemical analyses of the sediment were done so habitat differences couldn’t be evaluated. (Wang, 2007).
Beta proteobacteria have been consistently found in salt marshes. Ammonia-oxidizing bacteria (AOB) frequently identified associated with nitrification in salt marshes include Nitrosomonas and Nitrosospira, more specifically N.aestuarii, N. marina and N. ureae. Abundance varies along salinity gradients with both groups found in freshwater and Nitrosospira dominated in higher saline situations. Temperature, pH, net primary productivity and organic loading are also important factors in their distribution. Ammonia-oxidizing archaeal (AOA) appears to be more abundant than AOB in salt marshes with Crenarchaeota, being dominant. Similar to AOB, salinity, temperature, nitrite concentrations and net primary productivity are major factors in abundance. Increase in salinity appear to favor AOB but oxygen and C/N ratio also influence relative abundance with increasing oxygen and decreasing C/N favoring AOA. AOA abundance has also been linked to lead concentrations, percent clay and pH. (Bernhard, 2010). A major conclusion was that more research was needed into the nitrification role of AOA and AOB. (See Current Research.)
Sulfate Reducing Microbes
Crenarchaeal comprised over 70% of the archaeal clones recovered from three salt marsh sites dominated by different grasses. (Nelson, et al., 2009) Crenarchaeal are associated with sulfur rich environments. Euryarchaeaota have also been identified in salt marsh sediment. (Abreu, et al., 2001) Sulfur-reducing bacteria (SBR) are found in association with rhizosphere soils associated with Spartina, Phragmites and Scirpus grasses. Desulfobulbus, Desulfuromonas, Desulfovibrio, and Firmicutes were dominant. Comparing native plants (Phragmites and Scirpus) with invasive species (Spartina) higher richness and abundance of SRB were found during native plant vegetative growth and reproductive stages and were closely associated with decomposition of soil organic matter from the Spartina. (Nie,M. et al., 2009) Desulfuromonas Desulfovibrio
Primary producers found within the top few cm of sediment.
- Green algae
Decomposers are essential to the nutrient cycles for initiating carbon transfer through decomposition of grass organic matter. Fungi - Phaeosphaeria spartinicola (available links)
- Mycosphaerella sp.
- Phaeosphaeria halima.
Ammonia oxidizing bacteria and ammonia oxidizing archaea are critical in salt marshes in maintaining C:N ratio.
- Nitrosomonas Nitrosomonas
Sulfur reducing bacteria, sulfur reducing archaea and methanogenic archaea are primary producers utilizing the only available energy resources at deeper depths in the sediment where carbon is not available.
- Sulfur Reducing Bacteria
- Sulfur Reducing Archaea
- Methanogenic Archaea
Eukaryotes - Primary and secondary consumers graze on bacteria and fungi as well as predate on other eukarotic organisms.
Biodiversity and Ecosystem Functioning
A study of coastal lagoons has shown that environmental characteristics and bacterial diversity may not be related but a significant and positive correlation exist with the bacterial diversity and functioning efficiency of the lagoons. (Danovaro, 2007) Biodiversity and ecosystem functioning (BEF) may provide an indicator of subtle changes occurring in the habitat regardless of the source. Throughout the review of salt marsh processes there has been an emphasis on microbial community structure relationship to various geochemical gradients. Biodiversity has a significant impact on ability of the various processes to respond to changing conditions. Salt marshes may be one of the first indicators of global climate change. The dominant impact mean high water levels and mean higher high water levels have on various geochemical gradients and the subsequent impact on the associated microbial community may provide quantifiable shift in community structure with subtle change in sea level.
Salt Marsh Dieback
An increasing number of salt marsh “diebacks” (also known as “brown marsh”) have been reported of the last decade. These have occurred in coastal areas along the gulf coast and along the eastern coast from Florida to Maine. Initial studies indicated submergence was the primary cause. (Webb, 95) More recent studies have been less definitive and failed to find a single cause. Various explanations include sea level changes, drought, changes in soil chemistry, fungal pathogens, top-down consumer controls and multiple stressors. Further investigation is needed to unravel potential causes. (Alber, 2008). This may be another situation that would benefit from a BEF approach.
Heavy Metal Biological Cycling and Bioremediation
Environmental contamination of heavy metals has been an increasing problem with industrialization. Since salt marsh are recipients of wide ranging watershed areas the appearance of heavy metals is a natural outcome with salt marshes becoming sinks for these elements. In the presence of heavy metals (Zn, Cu, Cd, and Co), root tissue show major concentrations of heavy metals with negligible accumulation in the above ground tissue. A comparison response among Sarcocornia fruticosa, Sarcocornia perennis, Halimione portulacoides and Spartina maritime found a differential response with S. perennis providing the more effective phytoremediation. (Duarte, 2010) Another study found fungi to inhibit metal uptake. When concentrations of Fe, Cu, Mn and Pb uptake in Arthrocnemum macrostachyum and Sarcocornia fruticosa were analyzed in association with arbuscular mycorrhizal fungi, there was a negative correlation with the content of Pb and Zn in plant tissue. This suggests that fungi reduced the uptake of heavy metals in these plants. (Carrasco,2006) Further study of salt marshes may provide a better understanding of microbial community processes associated with bioremediation and heavy metal biological cycling.
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