Lateral Gene Transfer in a Heavy Metal-Contaminated-Groundwater Microbial Community

ABSTRACT Unraveling the drivers controlling the response and adaptation of biological communities to environmental change, especially anthropogenic activities, is a central but poorly understood issue in ecology and evolution. Comparative genomics studies suggest that lateral gene transfer (LGT) is a major force driving microbial genome evolution, but its role in the evolution of microbial communities remains elusive. To delineate the importance of LGT in mediating the response of a groundwater microbial community to heavy metal contamination, representative Rhodanobacter reference genomes were sequenced and compared to shotgun metagenome sequences. 16S rRNA gene-based amplicon sequence analysis indicated that Rhodanobacter populations were highly abundant in contaminated wells with low pHs and high levels of nitrate and heavy metals but remained rare in the uncontaminated wells. Sequence comparisons revealed that multiple geochemically important genes, including genes encoding Fe 2+ /Pb 2+ permeases, most denitrification enzymes, and cytochrome c 553 , were native to Rhodanobacter and not subjected to LGT. In contrast, the Rhodanobacter pangenome contained a recombinational hot spot in which numerous metal resistance genes were subjected to LGT and/or duplication. In particular, Co 2+ /Zn 2+ /Cd 2+ efflux and mercuric resistance operon genes appeared to be highly mobile within Rhodanobacter populations. Evidence of multiple duplications of a mercuric resistance operon common to most Rhodanobacter strains was also observed. Collectively, our analyses indicated the importance of LGT during the evolution of groundwater microbial communities in response to heavy metal contamination, and a conceptual model was developed to display such adaptive evolutionary processes for explaining the extreme dominance of Rhodanobacter populations in the contaminated groundwater microbiome. IMPORTANCE Lateral gene transfer (LGT), along with positive selection and gene duplication, are the three main mechanisms that drive adaptive evolution of microbial genomes and communities, but their relative importance is unclear. Some recent studies suggested that LGT is a major adaptive mechanism for microbial populations in response to changing environments, and hence, it could also be critical in shaping microbial community structure. However, direct evidence of LGT and its rates in extant natural microbial communities in response to changing environments is still lacking. Our results presented in this study provide explicit evidence that LGT played a crucial role in driving the evolution of a groundwater microbial community in response to extreme heavy metal contamination. It appears that acquisition of genes critical for survival, growth, and reproduction via LGT is the most rapid and effective way to enable microorganisms and associated microbial communities to quickly adapt to abrupt harsh environmental stresses.

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How the Soil Microbial Communities and Activities Respond to Long-Term Heavy Metal Contamination in Electroplating Contaminated Site

Microorganisms ◽

10.3390/microorganisms9020362 ◽

2021 ◽

Vol 9 (2) ◽

pp. 362 ◽

Cited By ~ 1

Author(s):

Wen-Jing Gong ◽

Zi-Fan Niu ◽

Xing-Run Wang ◽

He-Ping Zhao

Keyword(s):

Heavy Metal ◽

Microbial Communities ◽

Metal Contamination ◽

Heavy Metal Contamination ◽

Soil Microbial Communities ◽

Contaminated Site ◽

Rrna Gene ◽

Soil Microbial ◽

Cu And Zn

The effects of long-term heavy metal contamination on the soil biological processes and soil microbial communities were investigated in a typical electroplating site in Zhangjiakou, China. It was found that the soil of the electroplating plant at Zhangjiakou were heavily polluted by Cr, Cr (VI), Ni, Cu, and Zn, with concentrations ranged from 112.8 to 9727.2, 0 to 1083.3, 15.6 to 58.4, 10.8 to 510.0 and 69.6 to 631.6 mg/kg, respectively. Soil urease and phosphatase activities were significantly inhibited by the heavy metal contamination, while the microbial biomass carbon content and the bacterial community richness were much lower compared to noncontaminated samples, suggesting that the long-term heavy metal contamination had a severe negative effect on soil microorganisms. Differently, soil dehydrogenase was promoted in the presence of Chromate compared to noncontaminated samples. This might be due to the enrichment of Sphingomonadaceae, which have been proven to be able to secrete dehydrogenase. The high-throughput sequencing of the 16S rRNA gene documented that Proteobacteria, Actinobacteria, and Chloroflexi were the dominant bacterial phyla in the contaminated soil. The Spearman correlation analysis showed the Methylobacillus, Muribaculaceae, and Sphingomonadaceae were able to tolerate high concentrations of Cr, Cr (VI), Cu, and Zn, indicating their potential in soil remediation.

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Determining Rates of Change and Evaluating Group-Level Resiliency Differences in Hyporheic Microbial Communities in Response to Fluvial Heavy-Metal Deposition

Applied and Environmental Microbiology ◽

10.1128/aem.70.8.4756-4765.2004 ◽

2004 ◽

Vol 70 (8) ◽

pp. 4756-4765 ◽

Cited By ~ 24

Author(s):

Kevin P. Feris ◽

Philip W. Ramsey ◽

Matthias Rillig ◽

Johnnie N. Moore ◽

James E. Gannon ◽

...

Keyword(s):

Heavy Metals ◽

Heavy Metal ◽

Microbial Community ◽

Microbial Communities ◽

Metal Contamination ◽

Heavy Metal Contamination ◽

Indigenous Populations ◽

Curvilinear Relationship ◽

Group Level ◽

Rates Of Change

ABSTRACT Prior field studies by our group have demonstrated a relationship between fluvial deposition of heavy metals and hyporheic-zone microbial community structure. Here, we determined the rates of change in hyporheic microbial communities in response to heavy-metal contamination and assessed group-level differences in resiliency in response to heavy metals. A controlled laboratory study was performed using 20 flowthrough river mesocosms and a repeated-measurement factorial design. A single hyporheic microbial community was exposed to five different levels of an environmentally relevant metal treatment (0, 4, 8, 16, and 30% sterilized contaminated sediments). Community-level responses were monitored at 1, 2, 4, 8, and 12 weeks via denaturing gradient gel electrophoresis and quantitative PCR using group-specific primer sets for indigenous populations most closely related to the α-, β-, and γ-proteobacteria. There was a consistent, strong curvilinear relationship between community composition and heavy-metal contamination (R 2 = 0.83; P < 0.001), which was evident after only 7 days of metal exposure (i.e., short-term response). The abundance of each phylogenetic group was negatively affected by the heavy-metal treatments; however, each group recovered from the metal treatments to a different extent and at a unique rate during the course of the experiment. The structure of hyporheic microbial communities responded rapidly and at contamination levels an order of magnitude lower than those shown to elicit a response in aquatic macroinvertebrate assemblages. These studies indicate that hyporheic microbial communities are a sensitive and useful indicator of heavy-metal contamination in streams.

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

Applied and Environmental Microbiology ◽

10.1128/aem.70.4.2323-2331.2004 ◽

2004 ◽

Vol 70 (4) ◽

pp. 2323-2331 ◽

Cited By ~ 42

Author(s):

Kevin P. Feris ◽

Philip W. Ramsey ◽

Chris Frazar ◽

Matthias Rillig ◽

Johnnie N. Moore ◽

...

Keyword(s):

Heavy Metals ◽

Heavy Metal ◽

Community Structure ◽

Microbial Community ◽

Microbial Communities ◽

Microbial Community Structure ◽

Metal Contamination ◽

Hyporheic Zone ◽

Heavy Metal Contamination ◽

The Difference

ABSTRACT 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 α, β, and γ-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.

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

Applied and Environmental Microbiology ◽

10.1128/aem.69.9.5563-5573.2003 ◽

2003 ◽

Vol 69 (9) ◽

pp. 5563-5573 ◽

Cited By ~ 101

Author(s):

Kevin Feris ◽

Philip Ramsey ◽

Chris Frazar ◽

Johnnie N. Moore ◽

James E. Gannon ◽

...

Keyword(s):

Heavy Metal ◽

Community Structure ◽

Microbial Community ◽

Microbial Communities ◽

Microbial Community Structure ◽

Metal Contamination ◽

Metal Content ◽

Hyporheic Zone ◽

Heavy Metal Contamination ◽

Sediment Metal

ABSTRACT 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 α-, β-, and γ-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.

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