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Functional Responses of Salt Marsh Microbial Communities to Long-Term Nutrient Enrichment.

ABSTRACT:

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Environmental nutrient enrichment from human agricultural and waste runoff could cause changes to microbial communities that allow them to capitalize on newly available resources. Currently, the response of microbial communities to nutrient enrichment remains poorly understood, and, while some studies have shown no clear changes in community composition in response to heavy nutrient loading, others targeting specific genes have demonstrated clear impacts. In this study, we compared functional metagenomic profiles from sediment samples taken along two salt marsh creeks, one of which was exposed for more than 40 years to treated sewage effluent at its head. We identified strong and consistent increases in the relative abundance of microbial genes related to each of the biochemical steps in the denitrification pathway at enriched sites. Despite fine-scale local increases in the abundance of denitrification-related genes, the overall community structures based on broadly defined functional groups and taxonomic annotations were similar and varied with other environmental factors, such as salinity, which were common to both creeks. Homology-based taxonomic assignments of nitrous oxide reductase sequences in our data show that increases are spread over a broad taxonomic range, thus limiting detection from taxonomic data alone. Together, these results illustrate a functionally targeted yet taxonomically broad response of microbial communities to anthropogenic nutrient loading, indicating some resolution to the apparently conflicting results of existing studies on the impacts of nutrient loading in sediment communities.

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In this study, we used environmental metagenomics to assess the response of microbial communities in estuarine sediments to long-term, nutrient-rich sewage effluent exposure. Unlike previous studies, which have mainly characterized communities based on taxonomic data or primer-based amplification of specific target genes, our whole-genome metagenomics approach allowed an unbiased assessment of the abundance of denitrification-related genes across the entire community. We identified strong and consistent increases in the relative abundance of gene sequences related to denitrification pathways across a broad phylogenetic range at sites exposed to long-term nutrient addition. While further work is needed to determine the consequences of these community responses in regulating environmental nutrient cycles, the increased abundance of bacteria harboring denitrification genes suggests that such processes may be locally upregulated. In addition, our results illustrate how whole-genome metagenomics combined with targeted hypothesis testing can reveal fine-scale responses of microbial communities to environmental disturbance.

SUBMITTER: Graves CJ

PROVIDER: S-EPMC4836423 | biostudies-literature | 2016 May

REPOSITORIES: biostudies-literature

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Project description:Background and aimsEcosystem-based flood defence including salt-marsh as a key component is increasingly applied worldwide due to its multifunctionality and cost-effectiveness. While numerous experiments have explored the wave-attenuation effects of salt-marsh plants critical to flood protection, little is known about the physiological and biochemical responses of these species to continuous wave exposure.MethodsTo address this knowledge gap, we developed a shallow-water wave simulator to expose individual Spartina alterniflora plants to waves in a greenhouse for 8 weeks. S. alterniflora individuals were partially submerged and experienced horizontal sinusoidal motion to mimic plant exposure to shallow water waves. A factorial experiment was used to test the effects of three wave heights (4.1 cm, 5.5 cm and a no-wave control) and two wave periods (2 s and 3 s) on the following key physiological and biochemical plant parameters: plant growth, antioxidant defence and photosynthetic capacity.Key resultsComparison of wave treatment and control groups supported our hypotheses that wave exposure leads to oxidative stress in plants and suppresses plant photosynthetic capacity and thereby growth. In response, the wave-exposed plants exhibited activated antioxidant enzymes. Comparison between the different wave treatment groups suggested the wave effects to be generally correlated positively with wave height and negatively with wave period, i.e. waves with greater height and frequency imposed more stress on plants. In addition, wave-exposed plants tended to allocate more biomass to their roots. Such allocation is favourable because it enhances root anchorage against the wave impact.ConclusionsSimulated wave exposure systems such as the one used here are an effective tool for studying the response of salt-marsh plants to long-term wave exposure, and so help inform ecosystem-based flood defence projects in terms of plant selection, suitable transplantation locations and timing, etc. Given the projected variability of the global wave environment due to climate change, understanding plant response to long-term wave exposure has important implications for salt-marsh conservation and its central role in natural flood defence.

Project description:BackgroundSalt marshes are major natural repositories of sequestered organic carbon with high burial rates of organic matter, produced by highly productive native flora. Accumulated carbon predominantly exists as lignocellulose which is metabolised by communities of functionally diverse microbes. However, the organisms that orchestrate this process and the enzymatic mechanisms employed that regulate the accumulation, composition and permanence of this carbon stock are not yet known. We applied meta-exo-proteome proteomics and 16S rRNA gene profiling to study lignocellulose decomposition in situ within the surface level sediments of a natural established UK salt marsh.ResultsOur studies revealed a community dominated by Gammaproteobacteria, Bacteroidetes and Deltaproteobacteria that drive lignocellulose degradation in the salt marsh. We identify 42 families of lignocellulolytic bacteria of which the most active secretors of carbohydrate-active enzymes were observed to be Prolixibacteracea, Flavobacteriaceae, Cellvibrionaceae, Saccharospirillaceae, Alteromonadaceae, Vibrionaceae and Cytophagaceae. These families secreted lignocellulose-active glycoside hydrolase (GH) family enzymes GH3, GH5, GH6, GH9, GH10, GH11, GH13 and GH43 that were associated with degrading Spartina biomass. While fungi were present, we did not detect a lignocellulolytic contribution from fungi which are major contributors to terrestrial lignocellulose deconstruction. Oxidative enzymes such as laccases, peroxidases and lytic polysaccharide monooxygenases that are important for lignocellulose degradation in the terrestrial environment were present but not abundant, while a notable abundance of putative esterases (such as carbohydrate esterase family 1) associated with decoupling lignin from polysaccharides in lignocellulose was observed.ConclusionsHere, we identify a diverse cohort of previously undefined bacteria that drive lignocellulose degradation in the surface sediments of the salt marsh environment and describe the enzymatic mechanisms they employ to facilitate this process. Our results increase the understanding of the microbial and molecular mechanisms that underpin carbon sequestration from lignocellulose within salt marsh surface sediments in situ and provide insights into the potential enzymatic mechanisms regulating the enrichment of polyphenolics in salt marsh sediments. Video Abstract.

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Functional Responses of Salt Marsh Microbial Communities to Long-Term Nutrient Enrichment.

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