Microbial community evolution during simulated managed aquifer recharge in response to different biodegradable dissolved organic carbon (BDOC) concentrations

Abstract

This study investigates the evolution of the microbial community in laboratory-scale soil columns simulating the infiltration zone of managed aquifer recharge (MAR) systems and analogous natural aquifer sediment ecosystems. Parallel systems were supplemented with either moderate (1.1 mg/L) or low (0.5 mg/L) biodegradable dissolved organic carbon (BDOC) for a period of six months during which time, spatial (1 cm, 30 cm, 60 cm, 90 cm, and 120 cm) and temporal (monthly) analyses of sediment-associated microbial community structure were analyzed. Total microbial biomass associated with sediments was positively correlated with BDOC concentration where a significant decline in BDOC was observed along the column length. Analysis of 16S rRNA genes indicated dominance by Bacteria with Archaea comprising less than 1 percent of the total community. Proteobacteria was found to be the major phylum in samples from all column depths with contributions from Betaproteobacteria, Alphaproteobacteria and Gammaproteobacteria. Microbial community structure at all the phylum, class and genus levels differed significantly at 1 cm between columns receiving moderate and low BDOC concentrations; in contrast strong similarities were observed both between parallel column systems and across samples from 30 to 120 cm depths. Samples from 1 cm depth of the low BDOC columns exhibited higher microbial diversity (expressed as Shannon Index) than those at 1 cm of moderate BDOC columns, and both increased from 5.4 to 5.9 at 1 cm depth to 6.7–8.3 at 30–120 cm depths. The microbial community structure reached steady state after 3–4 months since the initiation of the experiment, which also resulted in an improved DOC removal during the same time period. This study suggested that BDOC could significantly influence microbial community structure regarding both composition and diversity of artificial MAR systems and analogous natural aquifer sediment ecosystems.

Introduction

Managed aquifer recharge (MAR) systems have been used globally for decades to enhance the availability of localized water supplies; they include riverbank filtration, soil-aquifer treatment and aquifer recharge and recovery (Ray et al., 2008). These systems can utilize less desirable water sources such as storm water, impaired surface water, and reclaimed water to recharge groundwater and to augment drinking water supplies (Ray et al., 2008; Missimer et al., 2011). Increasing population growth, limited pristine water supplies and climatic shifts suggest that the application of MAR will increase in arid and semi-arid regions in the future.

In addition to storage, MAR can play an important role in water treatment. Aquifer sediments in the vadose and saturated zones act as a natural filter for removing nutrients, bulk organic matter, disinfection by-product precursors, trace organic chemicals and pathogens as water percolates through the subsurface in all MAR systems. Many biogeochemical and hydrogeological parameters can influence these attenuation processes. Of particular interest in this study is the characteristics of the indigenous microbial community since microbial degradation and assimilation can play a dominant role in the attenuation of diverse organic compounds which include many recalcitrant trace organic chemicals of emerging concern (Amy and Drewes, 2007). Thus, a thorough understanding of the microbial population in aquifer sediments is important for elucidating our mechanistic understanding and improving the performance of MAR systems.

Meanwhile, a better understanding of microbial ecology in MAR will also improve our understanding of diverse biogeochemical processes in analogous natural ecosystems including freshwater, aquifer sediments and groundwater. Dissolved organic compounds introduced into these types of ecosystems mainly originate from autochthonous sources such as phytoplankton production (Fogg, 1983) and allochthonous sources such as wastewater (Lennon and Pfaff, 2005). It has been estimated that global freshwater sediments receive organic carbon at 0.2 Pg annually (Cole et al., 2007), which are either buried in sediments or percolate downward through sediments and reach groundwater accompanying with significant biodegradation during the whole process. The mineralization of organic compounds by indigenous heterotrophic microorganisms in aquifer sediments and the microbial community in this ecosystem deserves more detailed characterization.

Some research has been conducted regarding the composition, dynamic changes, function, and resistance to environmental perturbation of microbial communities in sediments (Blume et al., 2002; Holden and Fierer, 2005; Rauch-Williams and Drewes, 2006; Hansel et al., 2008; Yagi et al., 2010; Foulquier et al., 2011). The results indicated that total biomass was positively correlated to dissolved organic carbon (DOC), and microbial community composition can be influenced by many factors including depth, DOC, water content and pH. However, as DOC is just a general parameter, more details about the influence of biodegradable DOC (BDOC) and organic matter composition on microbial community remain unknown until now. Although sediments and soils are believed to harbor the highest diversity of microbial residents on earth (Torsvik et al., 1990), the details of microbial community composition and evolution in freshwater sediments, particularly engineered aquifer recharge systems, is not yet well understood. Previous research has relied primarily on molecular fingerprinting methods with comparably low resolution (i.e. denaturing gradient gel electrophoresis) that is inadequate to discern minor groups in these systems. More powerful fingerprinting techniques with higher resolution, such as high throughput barcoded sequencing of 16S and 18S rRNA genes of prokaryotes and eukaryotes have now been adopted in diverse ecosystems (Roesch et al., 2007; Galand et al., 2009; Benson et al., 2010; Zhang et al., 2010; Caporaso et al., 2011); these techniques hold immense promise for providing a more detailed understanding of the microbial community in aquifer sediments.

In this study, we establish and investigate a series of laboratory-scale sediment columns to simulate the microbial ecology associated with labile dissolved organic compounds in MAR and analogous natural settings. Laboratory-scale sediment columns have historically been utilized to simulate diverse biological and physicochemical processes in aquifer sediments in order to better understand overall performance (Bellin and Rao, 1993). The level of control available in the laboratory enables a level of clarity and sampling access not available in field-scale research. Since prior work suggests that DOC is a major factor influencing microbial community structure in sediments (Bossio and Scow, 1995; Zhou et al., 2002; Li et al., 2012), two sets of laboratory columns receiving different DOC and BDOC concentrations were employed to explore microbial ecology and responses to DOC availability. The evolution of sediment associated microorganisms were then tracked for six months of operation. The results of this temporal and spatial series can elucidate the dynamic process of microbial communities in engineered aquifer recharge systems and analogous natural sediment ecosystems such as hyporheic zones or wetlands. It also provides important operational information regarding the necessary time to achieve a stable microbial community in MAR systems.