Effects of vegetation on root-associated microbial communities: A comparison of disturbed versus undisturbed estuarine sediments

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Abstract

While it has been demonstrated that microbial communities are influenced by plant species composition in upland systems, less is known about how estuarine vegetation may influence the structure and functional capabilities of sediment microbial communities. In this study, we adapted terrestrial catabolic response profile (CRP) methods for use under brackish anaerobic conditions. CRPs were employed to determine whether salt marsh vegetation had an effect on sediment microbial community function. Phospholipid fatty acids (PLFAs) were utilized as a descriptor of microbial community structure. Samples were obtained from monospecific Spartina alterniflora and Phragmites australis plots located in disturbed and undisturbed estuarine salt marsh systems. In response to the addition of a range of 30 organic substrates we observed significant CO2 production in vegetated versus non-vegetated sediments from the undisturbed site. Vegetated sediments from the undisturbed system produced greater amounts of both CO2 and CH4, while sediments from the disturbed site consumed CO2 except in response to carboxylic acid substrates. In response to nitrogen-containing (amino acid) substrates undisturbed Phragmites sediments produced the highest amount of CO2 seen in any sample. Few differences in CRPs or PLFAs were seen in sediments from the disturbed site. The production of CO2 was significantly correlated with microbial community structure as described by PLFA profiles. This study is the first to use CRPs to describe estuarine sediment microbial community functional ability, and to link this ability with community PLFA composition. Our results suggest that individual plant species have a less pronounced effect than has been observed in upland soils in structuring salt marsh sediment microbial communities. Under anthropogenically disturbed conditions the effects of the macrophyte root zone on the sediment microbial communities may be overwhelmed, resulting in different ecosystem level functional abilities.

Introduction

In terrestrial soils, the composition and functional abilities of microbial communities are influenced by their association with specific plant species (Ehrenfeld et al., 2005; Grayston et al., 1998, Grayston et al., 2001; Marschner et al., 2001; Boschker et al., 1999). Studies in diverse ecosystems (peatlands—Borga et al., 1994; forests and grasslands—Kourtev et al., 2003; Degens and Harris, 1997; agricultural—Schutter and Dick, 2001) have shown plant species composition to be an important factor, both in selecting for specific microbial populations and in influencing the diversity and functional capacity of these communities. These soil microbial communities provide ecosystem level functions such as the decomposition of soil organic matter (SOM), and variations in microbial decomposition rates have been associated with different plant species (Kourtev et al., 2003; Boschker et al., 1999; Liljeroth et al., 1994).

Differences in microbial numbers, community composition, and variations in nutrient cycling activities and contaminant transformations have also been observed in salt marsh microbial communities associated with vegetation (Ravit et al., 2003, Ravit et al., 2005; Burke et al., 2002; Nielsen et al., 2001; Bagwell et al., 2001; Daane et al., 2001; Hines et al., 1999). However, few studies of either estuarine vegetation or microbiota have compared the effect of different macrophyte species on biogeochemical functions that occur in brackish sediments. In the highly organic sediments often encountered in wetlands (Richert et al., 2000) a large pool of belowground dead biomass and labile organic compounds excreted by live plant roots support microbial activity. Root transfer of oxygen (O2) from the atmosphere to the rhizosphere is well documented (Armstrong et al., 1996; Grosse et al., 1996; Mendelssohn et al., 1981; Teal and Kanwisher, 1966). While root-derived carbon (C) may be a less important factor in highly organic estuarine sediments than in upland mineral soils, the root-derived O2 inputs may be an important influence in determining microbial community composition (Ludemann et al., 2000). Because estuarine plant species differ in their root biomass, turnover, exudation, and O2 leakage, it can be expected that macrophyte vegetation contributes to the structuring of these sediment microbial communities.

The increasing dominance of Phragmites australis (Cav.) Trin. ex. Steud. (hereafter Phragmites) in brackish estuarine marshes of the northeastern US has sparked extensive efforts to restore Spartina species to tidal marshes (Meyerson et al., 2000; Rooth and Stevenson, 2000; Rice et al., 2000). Restoration efforts are often justified in terms of lost or altered ecosystem functions associated with the Phragmites invasions. While these restoration efforts have stimulated many studies of the comparative ability of Phragmites and Spartina to support vertebrate and invertebrate fauna (Weis and Weis, 2000; Wainwright et al., 2000; Weinstein and Balletto, 1999), relatively little attention has been paid to a comparison of the microbial communities associated with the root zones of these two plant species. The dissimilar root morphologies and processes of root oxidation in Phragmites and Spartina alterniflora (hereafter Spartina) can result in differences in characteristics of the sediments associated with these two plants (Armstrong et al., 2000; Windham and Lathrop, 1999; Chambers, 1997; Hwang and Morris, 1991), and these differences may be a factor in structuring sediment microbial communities.

Catabolic response profiles (CRPs) measure CO2 production after the addition of a range of simple substrates, and this technique has been used to differentiate microbial ability to mineralize various organic compounds and to describe microbial functional diversity in upland soils (Kourtev et al., 2003; Degens et al., 2001; Degens, 1999; Degens and Harris, 1997). However, this approach has not yet been used in the highly organic anaerobic sediments typical of salt marshes. CRP substrates include a range of organic compounds (carboxylic and amino acids, simple sugars, complex polymers) and a short incubation time (2–3 h) that more closely reflects in situ microbial activity, thus minimizing the selective biases associated with microbial culturing techniques (Øvreås, 2000).

Our study modified the procedures of Degens and Harris (1997) for use under anaerobic conditions. Substrate concentrations were chosen for preliminary experiments from a range of 90 organic compounds found in roots growing under anaerobic conditions [based on the studies of Campbell et al. (1997), Gopal and Goel (1993), Bertani and Reggiani (1991), and Crawford (1980)]. Various substrate concentrations were tested at multiple incubation time intervals. From these experiments we determined the substrates that produced measurable responses under anaerobic conditions during 3–4 h benchtop incubation. During these initial studies we observed that the addition of certain substrates resulted in a reduction in CO2 with respect to the sediment control (addition of 1 ml deionized H2O only), and so added the analysis of methane (CH4) to our methods.

Our experimental goal was to determine whether the Phragmites and Spartina root zones supported different microbial communities, and whether anthropogenic disturbance overrides the effects of these plants on the sediment microbiota. A second goal was to determine whether microbial functionality in anaerobic sediments (as measured by CRPs) could be linked to microbial community structure as described by phospholipid fatty acids (PLFAs), molecular biomarkers that have been used extensively to describe microbial communities in soils and sediments (Ravit et al., 2005; Kourtev et al., 2003; Ibekwe and Kennedy, 1998; Borga et al., 1994; White et al., 1979).

Section snippets

Sediment samples

Root-associated sediment samples were obtained from adjacent populations of Phragmites australis and Spartina alterniflora and unvegetated intertidal mudflats in two New Jersey coastal marshes. The first site, Saw Mill Creek (SMC) in the Hackensack Meadowlands, has a lengthy history of disturbance. Anthropogenic inputs of a variety of industrial contaminants including heavy metals, chlorinated hydrocarbons, polycyclic aromatic hydrocarbons, and other toxic compounds (Kennish, 1992), as well as

Sediment characteristics

Sediment characteristics were quite similar between the sites and species, and the observed values are within the range of variability typically observed both within and between brackish marshes (Table 1). Within the undisturbed MAUR site small, but statistically significant differences, in SOM and pH were observed between vegetated and unvegetated sediments. There were no statistically significant differences between vegetated and unvegetated sediments within the SMC site. As expected, SOM was

Discussion

Contrary to expectation, the sediment microbial communities associated with two estuarine plant species could not be separated by either indices of community structure (PLFAs) or community function (CRPs). We found that sediment microbial community structure and function reflected primarily the conditions of the specific sites that were sampled. Both the structural and functional indices differentiated the vegetated and unvegetated communities at the undisturbed MAUR site, but not at the

Acknowledgements

Funding for B. Ravit was provided by USEPA STAR, NSF-DDIG, and the New Jersey Water Resources Research Institute (NJWRRI). We gratefully acknowledge the invaluable assistance of Mike Bartels, Jared Eudell, and Steve Eisenhower for their help in field sampling. We thank Hackensack Riverkeeper and the Natural Lands Trust for providing transportation to the field sites (SMC and MAUR, respectively).

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