mmobilization and bacterial utilization of dissolved organic carbon entering the riparian zone of the alpine Enns River, Austria

142

The hyporheic zone of a river is nonphotic, has steep chemical and redox gradients, and has a heterotrophic food web based on the consumption of organic carbon entrained from downwelling surface water or from upwelling groundwater. The microbial communities in the hyporheic zone are an important component of these heterotrophic food webs and perform essential functions in lotic ecosystems. Using a suite of methods (denaturing gradient gel electrophoresis, 16S rRNA phylogeny, phospholipid fatty acid analysis, direct microscopic enumeration, and quantitative PCR), we compared the microbial communities inhabiting the hyporheic zone of six different river sites that encompass a wide range of sediment metal loads resulting from large base-metal mining activity in the region. There was no correlation between sediment metal content and the total hyporheic microbial biomass present within each site. However, microbial community structure showed a significant linear relationship with the sediment metal loads. The abundances of four phylogenetic groups (groups I, II, III, and IV) most closely related to ␣-, ␤-, and ␥-proteobacteria and the cyanobacteria, respectively, were determined. The sediment metal content gradient was positively correlated with group III abundance and negatively correlated with group II abundance. No correlation was apparent with regard to group I or IV abundance. This is the first documentation of a relationship between fluvially deposited heavy-metal contamination and hyporheic microbial community structure. The information presented here may be useful in predicting long-term effects of heavy-metal contamination in streams and provides a basis for further studies of metal effects on hyporheic microbial communities.The hyporheic zone is a spatially and temporally dynamic ecotone which provides connectivity between terrestrial, groundwater, and lotic habitats (12,31,69,72,73). It lies beneath the channel of a stream (46), often extending great distances laterally in the subsurface, and is an essential part of lotic ecosystems (22,57,59). The microbial transformations of dissolved and particulate nutrients taking place in the hyporheic zone have been shown to influence both macroinvertebrate and algal assemblages and may play a role in the productivity of riparian vegetation (4,36,58). Therefore, alterations in the hyporheic ecosystem that result in changes in the resident microbial community structure may be translated to higher trophic levels. In addition, alterations in the structure of microbial communities may be a useful indicator of the effects and extent of anthropogenic contamination. Previous work in our laboratory has focused on describing the types and seasonal dynamics of microorganisms in the hyporheic zone (21). This investigation explores the effects of heavy-metal contamination on hyporheic-zone microbial community structure.Heavy metals contaminate numerous aquatic environments worldwide as a result of large-scale mining and other activities (49). Heavy metals reduce water quality a...

Section: Methodsmentioning

confidence: 94%

“…It is acknowledged that predation (33,38) and dissolved-organic-carbon quality and quantity (11,25,56,79) can have effects on the size and structure of microbial communities. Determining the effects of the former was beyond the scope of this investigation, and dissolved-organic-carbon levels VOL.…”

Section: Discussionmentioning

confidence: 99%

Differences in Hyporheic-Zone Microbial Community Structure along a Heavy-Metal Contamination Gradient

Feris

Ramsey

Frazar

et al. 2003

142

“…However, previous studies in other streams have identified exogenous organic carbon as an important growth substrate for bacteria in the hyporheic zone (10,29,59). The majority of exogenous organic carbon that enters lotic ecosystems in this montane region arrives during the fall and early winter, primarily through deposition of leaf litter (18,59).…”

Section: Discussionmentioning

confidence: 99%

“…This coarse organic matter is processed by aquatic insects, fungi, and bacteria and is eventually entrained in the hyporheic zone as dissolved organic carbon (48,67). Entrainment of dissolved organic carbon normally promotes increased respiration and growth in hyporheic microbial communities (10,29,59). Thus, elevated heavy-metal levels in the hyporheic zone appear to inhibit the growth of group I and II organisms during the fall and early winter, when conditions may otherwise favor their growth.…”

Section: Discussionmentioning

confidence: 99%

Seasonal Dynamics of Shallow-Hyporheic-Zone Microbial Community Structure along a Heavy-Metal Contamination Gradient

Feris

Ramsey

Frazar

et al. 2004

Heavy metals contaminate numerous freshwater streams and rivers worldwide. Previous work by this group demonstrated a relationship between the structure of hyporheic microbial communities and the fluvial deposition of heavy metals along a contamination gradient during the fall season. Seasonal variation has been documented in microbial communities in numerous terrestrial and aquatic environments, including the hyporheic zone. The current study was designed to assess whether relationships between hyporheic microbial community structure and heavy-metal contamination vary seasonally by monitoring community structure along a heavy-metal contamination gradient for more than a year. No relationship between total bacterial abundance and heavy metals was observed (R 2 ‫؍‬ 0.02, P ‫؍‬ 0.83). However, denaturing gradient gel electrophoresis pattern analysis indicated a strong and consistent linear relationship between the difference in microbial community composition (populations present) and the difference in the heavy metal content of hyporheic sediments throughout the year (R 2 ‫؍‬ 0.58, P < 0.001). Correlations between heavy-metal contamination and the abundance of four specific phylogenetic groups (most closely related to the ␣, ␤, and ␥-proteobacteria and cyanobacteria) were apparent only during the fall and early winter, when the majority of organic matter is deposited into regional streams. These seasonal data suggest that the abundance of susceptible populations responds to heavy metals primarily during seasons when the potential for growth is highest.Large-scale mining and other activities have resulted in contamination of many aquatic environments around the world (50). Changes in the geochemical characteristics of heavy-metal-contaminated environments are well documented (for a review, see Moore and Luoma [50]). Heavy-metal contamination can reduce water quality and has been shown to harm numerous organisms (12,45,50,69). Several studies have examined the effects of this type of anthropogenic contamination on aquatic macrobiota (1, 12-15, 33, 47). While heavy-metal effects on the activity and composition of microbial communities in terrestrial ecosystems have been well documented (2,6,7,20,21,34,43,49,54,64,72), relatively little is known about the effects on aquatic microbial communities. In a prior study by our group, heavy-metal contamination was implicated as a structuring factor for hyporheic microbial communities in streambeds (23).The hyporheic zone is the region of heterogeneous sediments beneath and adjacent to the stream channel that is saturated with a mixture of surface and ground water (46), providing connectivity between terrestrial, groundwater, and lotic habitats. As such, this zone is an important component of lotic ecosystems (11,26,35,58,60,68,70,71). The microbial communities in the hyporheic zone play important functional roles in lotic environments (18,31,32,51,52,57,59). For example, transformation of dissolved and particulate nutrients by hyporheic microorganisms can influence the distr...

“…The correlation between DOC concentration and the community structure of the epilithic, but not the sediment, community suggests that sources of organic carbon supporting secondary productivity partition differently between these two streambed habitats (42,54,56). While the epilithic populations are generally limited to dissolved carbon in the bulk flow and endogenous carbon (DOC and POC derived from the biofilm), the sediment populations likely obtain additional resources from entrained POC and DOC upwelling from the hyporheic zone (5,10,30,54). The appearance of both prokaryotic and eukaryotic primary producers in the epilithon during the summer months suggests a seasonal shift towards autocthonous carbon sources within this biofilm, as is also supported by prior estimates of autochthonous primary productivity in White Clay Creek (31).…”

Section: Discussionmentioning

confidence: 99%

Recurring Seasonal Dynamics of Microbial Communities in Stream Habitats

Hullar

Kaplan

Stahl

2006

160

128

Recurring seasonal patterns of microbial distribution and abundance in three third-order temperate streams within the southeast Pennsylvania Piedmont were observed over 4 years. Populations associated with streambed sediments and rocks (epilithon) were identified using terminal restriction length polymorphism (tRFLP) and sequencing of 16S rRNA genes selectively amplified with primers for the bacterial domain. Analyses of the relative magnitudes of tRFLP peak areas by using nonmetric multidimensional scaling resolved clear seasonal trends in epilithic and sediment populations. Oscillations between two dominant groups of epilithic genotypes, explaining 86% of the seasonal variation in the data set, were correlated with temperature and dissolved organic carbon. Sequences affiliated with epilithic phototrophs (cyanobacteria and diatom chloroplasts), a Rhodoferax sp., and a Bacillus species clustered in the summer, whereas sequences most closely related to "Betaproteobacteria" (putative Burkholderia sp.), and a putative cyanobacterium clustered in the fall/spring. The sediment genotypes also clustered into two groups, and these explained 85% of seasonal variation but correlated only with temperature. A summer tRFLP pattern was characterized by prevalence of "Betaproteobacteria," "Gammaproteobacteria," and a Bacillus sp., whereas the winter/spring pattern was characterized by phylotypes most closely related to "Firmicutes," "Gammaproteobacteria," and "Nitrospirae." A close association between these headwater streams and their watersheds was suggested by the recovery of sequences related to microbial populations provisionally attributed to not only freshwaters but also terrestrial habitats.Headwater streams are a primary link between aquatic and terrestrial ecosystems, transforming and exporting terrestrially derived materials and also contributing to export through autochthonous primary production. Complex communities of macro-and microbiota distributed among different stream habitats primarily mediate these transformations. The trophic structures of stream macrobiota and phototrophic eukaryotic microbiota have been intensively studied as contributors to production and energy flow in lotic systems (26). In contrast, although microorganisms exert significant, if not major, control on system chemistry and the processing of terrestrial inputs, there is little understanding of differences in lotic microbial population structure among biomes, population similarity among streams within a biome, or changes in structure associated with seasonal oscillations in chemical and physical parameters. This information is essential for developing a more complete description of the trophic structure and biogeochemistry of streams, one that more fully incorporates their relationship to the proximal terrestrial system (11,12,16,47,48).Microbial communities in the temperate deciduous forest biome are exposed to seasonal changes in their chemical and physical environments. Some seasonal changes are constrained, such as variation in light a...