Fluctuations in Species-Level Protein Expression Occur during Element and Nutrient Cycling in the Subsurface

Wilkins, Michael J.; Wrighton, Kelly; Nicora, Carrie; Williams, Kenneth H.; McCue, Lee Ann; Handley, Kim M.; Miller, Christopher S.; Giloteaux, Ludovic; Montgomery, Alison P.; Lovley, Derek R.; Banfield, Jillian F.; Long, Philip E.; Lipton, Mary

doi:10.1371/journal.pone.0057819

Cited by 19 publications

(21 citation statements)

References 38 publications

(50 reference statements)

Supporting

Mentioning

Contrasting

Order By: Relevance

“…The expression of Geobacter-affiliated uptake hydrogenase gene detected here is consistent with proteomic investigations from other acetate stimulations at the site, where the authors concluded hydrogen may be a donor for metal reduction (Wilkins et al, 2013). From the ACD data, we detected greater proteomic support for H 2 production relative to other fermentation end products (Figure 4).…”

Section: Metabolic Interdependencies In An Aquifer Microbial Communitsupporting

confidence: 88%

Metabolic interdependencies between phylogenetically novel fermenters and respiratory organisms in an unconfined aquifer

et al. 2014

View full text Add to dashboard Cite

Fermentation-based metabolism is an important ecosystem function often associated with environments rich in organic carbon, such as wetlands, sewage sludge and the mammalian gut. The diversity of microorganisms and pathways involved in carbon and hydrogen cycling in sediments and aquifers and the impacts of these processes on other biogeochemical cycles remain poorly understood. Here we used metagenomics and proteomics to characterize microbial communities sampled from an aquifer adjacent to the Colorado River at Rifle, CO, USA, and document interlinked microbial roles in geochemical cycling. The organic carbon content in the aquifer was elevated via acetate amendment of the groundwater occurring over 2 successive years. Samples were collected at three time points, with the objective of extensive genome recovery to enable metabolic reconstruction of the community. Fermentative community members include organisms from a new phylum, Melainabacteria, most closely related to Cyanobacteria, phylogenetically novel members of the Chloroflexi and Bacteroidales, as well as candidate phyla genomes (OD1, BD1-5, SR1, WWE3, ACD58, TM6, PER and OP11). These organisms have the capacity to produce hydrogen, acetate, formate, ethanol, butyrate and lactate, activities supported by proteomic data. The diversity and expression of hydrogenases suggests the importance of hydrogen metabolism in the subsurface. Our proteogenomic data further indicate the consumption of fermentation intermediates by Proteobacteria can be coupled to nitrate, sulfate and iron reduction. Thus, fermentation carried out by previously unknown members of sediment microbial communities may be an important driver of nitrogen, hydrogen, sulfur, carbon and iron cycling.

show abstract

Section: Metabolic Interdependencies In An Aquifer Microbial Communitsupporting

confidence: 88%

Metabolic interdependencies between phylogenetically novel fermenters and respiratory organisms in an unconfined aquifer

et al. 2014

View full text Add to dashboard Cite

show abstract

“…that bloom when acetate is added to groundwater at the Rifle, Colorado study site to promote in situ uranium bioremediation , previous studies of the microbial community that employed a global proteomics approach, detected few, if any, c-type cytochromes (Wilkins et al, , 2013Callister et al, 2010). As an alternative heme-specific approach, proteins extracted from groundwater samples collected during two in situ bioremediation experiments were separated with SDS-PAGE and visualized with heme staining.…”

Section: Resultsmentioning

confidence: 99%

“…contain a large number of c-type cytochromes , but previous proteomic studies of the microbial community during in situ uranium bioremediation sites, identified few, if any, c-type cytochromes (Wilkins et al, , 2013Callister et al, 2010). One reason for this may be the poor conservation of c-type cytochromes in Geobacter sp.…”

Section: Introductionmentioning

confidence: 98%

Functional environmental proteomics: elucidating the role of a c-type cytochrome abundant during uranium bioremediation

et al. 2015

View full text Add to dashboard Cite

Studies with pure cultures of dissimilatory metal-reducing microorganisms have demonstrated that outer-surface c-type cytochromes are important electron transfer agents for the reduction of metals, but previous environmental proteomic studies have typically not recovered cytochrome sequences from subsurface environments in which metal reduction is important. Gel-separation, heme-staining and mass spectrometry of proteins in groundwater from in situ uranium bioremediation experiments identified a putative c-type cytochrome, designated Geobactersubsurface c-type cytochrome A (GscA), encoded within the genome of strain M18, a Geobacter isolate previously recovered from the site. Homologs of GscA were identified in the genomes of other Geobacter isolates in the phylogenetic cluster known as subsurface clade 1, which predominates in a diversity of Fe(III)-reducing subsurface environments. Most of the gscA sequences recovered from groundwater genomic DNA clustered in a tight phylogenetic group closely related to strain M18. GscA was most abundant in groundwater samples in which Geobacter sp. predominated. Expression of gscA in a strain of Geobacter sulfurreducens that lacked the gene for the c-type cytochrome OmcS, thought to facilitate electron transfer from conductive pili to Fe(III) oxide, restored the capacity for Fe(III) oxide reduction. Atomic force microscopy provided evidence that GscA was associated with the pili. These results demonstrate that a c-type cytochrome with an apparent function similar to that of OmcS is abundant when Geobacter sp. are abundant in the subsurface, providing insight into the mechanisms for the growth of subsurface Geobacter sp. on Fe(III) oxide and suggesting an approach for functional analysis of other Geobacter proteins found in the subsurface.

show abstract

“…Increased flux of organic carbon or the introduction of a specific carbon compound during this event may offer an opportunity for fast-growing bacterial species to out-compete potential K-strategists such as Pedobacter species. The ability of specific bacterial groups to rapidly increase in abundance in response to changing organic carbon flux has been previously demonstrated in an analogous environment (Wilkins et al, 2013). Better characterizing chemical (carbon, sulfur, nitrogen species) shifts associated with Columbia River water intrusion into the Hanford aquifer will therefore be essential for identifying geochemical drivers of microbial community change.…”

Section: Potential Links To Local Hydrologymentioning

confidence: 93%

Single-cell genomics reveals metabolic strategies for microbial growth and survival in an oligotrophic aquifer

et al. 2014

Self Cite

View full text Add to dashboard Cite

Bacteria from the genus Pedobacter are a major component of microbial assemblages at Hanford Site (a largely decommissioned nuclear production complex) in eastern Washington state, USA, and have been shown to change significantly in abundance in response to the subsurface intrusion of Columbia River water. Here we employed single-cell genomics techniques to shed light on the physiological niche of these micro-organisms. Analysis of four Pedobacter single amplified genomes (SAGs) from Hanford Site sediments revealed a chemoheterotrophic lifestyle, with the potential to exist under both aerobic and microaerophilic conditions via expression of both aa3 -type and cbb3 -type cytochrome c oxidases. These SAGs encoded a wide range of both intra- and extracellular carbohydrate-active enzymes, potentially enabling the degradation of recalcitrant substrates such as xylan and chitin, and the utilization of more labile sugars such as mannose and fucose. Coupled to these enzymes, a diversity of transporters and sugar-binding molecules were involved in the uptake of carbon from the extracellular local environment. The SAGs were enriched in TonB-dependent receptors, which play a key role in uptake of substrates resulting from degradation of recalcitrant carbon. Clustered Regularly Interspaced Short Palindromic Repeat (CRISPR)-Cas mechanisms for resisting viral infections were identified in all SAGs. These data demonstrate the potential mechanisms utilized for persistence by heterotrophic micro-organisms in a carbon-limited aquifer, and hint at potential linkages between observed Pedobacter abundance shifts within the 300 Area (in the south-eastern corner of the site) subsurface and biogeochemical shifts associated with Columbia River water intrusion.

show abstract

Fluctuations in Species-Level Protein Expression Occur during Element and Nutrient Cycling in the Subsurface

Cited by 19 publications

References 38 publications

Metabolic interdependencies between phylogenetically novel fermenters and respiratory organisms in an unconfined aquifer

Metabolic interdependencies between phylogenetically novel fermenters and respiratory organisms in an unconfined aquifer

Functional environmental proteomics: elucidating the role of a c-type cytochrome abundant during uranium bioremediation

Single-cell genomics reveals metabolic strategies for microbial growth and survival in an oligotrophic aquifer

Contact Info

Product

Resources

About