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Silver, W. L.

Publications and source records attributed to Silver, W. L..

5 recordsLinked to original sources

Microbial communities in tropical soils are highly resilient to fluctuating redox conditions

Many wet tropical soils alternate frequently between fully oxygenated and anaerobic conditions, constraining the terminal electron acceptors available for microbial metabolism, and the mineral-organic matter interactions that regulate many aspects of soil carbon (C) cycling. However, it is still unclear how fluctuating soil redox conditions influence the microbial community composition and if microbially mediated C flux is sensitive to extended oxic or anoxic periods like those observed during drought and flooding respectively. Using a 44-day redox manipulation of tropical soils that experience daily-to-weekly oxygen (O2) fluctuations in the field, we measured how different redox regimes shape soil biogeochemistry and microbial and metabolite composition. Replicate microcosms were exposed to four treatments (static oxic, static anoxic, high frequency fluctuation (4 day oxic/4 day anoxic), or low frequency fluctuation (8 day oxic/4 day anoxic)) regimes, and harvested for microbial, metabolite, carbon dioxide (CO2) flux, and biogeochemical assays at multiple timepoints. Oxic and fluctuating redox conditions caused the microbial community to shift in a manner correlated with soil iron content and directly orthogonal to communities from anoxic soils. The identity of both iron oxidizers and iron reducers was distinct in static anoxic soils but was resilient to redox fluctuation and prolonged O2 exposure. The total amount of CO2 respired was similar across all four redox regimes. Water-extractable organic matter composition was distinct across redox treatments, with anoxic soils accumulating higher levels of carbohydrate-, proteins-, amino sugar-, and lignin-like compounds consistent with reduced enzymatic decomposition and release of mineral-associated organic matter via iron reduction, while oxic soils showed elevated lipid- and unsaturated hydrocarbon-like compounds indicative of greater microbial biomass turnover. The microbial community adapted to dynamic redox conditions and the results substantiate cycling of distinct C compounds under varying redox conditions resulting from varying bioavailability (driven by mineral-OM dynamics) and/or shifted microbial metabolism.

microbiology↗

Mechanisms of carbon dioxide detection in the earthworm Dendrobaena veneta.

Carbon dioxide (CO2) is a critical biological signal that is noxious to many animals at high concentrations. The earthworm Dendrobaena veneta lives in subterranean burrows containing high levels of CO2 and respires through its skin. Despite the ecological and agricultural importance of earthworms, relatively little is known about how they make decisions in their environment, including their response to elevated levels of CO2. To examine CO2 detection in this species, we designed the exudate assay, in which we placed an earthworm in a sealed container, exposed it to varying concentrations of CO2 for one minute, and recorded the amount of exudate secreted. Because earthworms excrete exudate in response to noxious stimuli, we hypothesized that the amount of exudate produced was proportional to the amount of irritation. We repeated these experiments after treatment with several blockers for molecules with potential involvement in CO2 detection, including carbonic anhydrases, guanylate cyclase, TRPA1, ASICs, and OTOP channels. We also confirmed the presence of homologous transcripts for each of these gene families in an epithelial transcriptome for D. veneta. Additionally, since organisms often detect CO2 levels indirectly by monitoring the conversion to carbonic acid (a weak acid), we used the exudate assay to evaluate aversion to additional weak acids (formic acid, acetic acid, and propionic acid). Earthworms excreted significantly more exudate in response to CO2 in a dosage-dependent manner, and this response was muted by the general carbonic anhydrase inhibitor acetazolamide, the carbonic anhydrase IX/XII inhibitor indisulam, the calcium channel blocker ruthenium red, the sodium channel blocker amiloride, and the acid-sensing ion channel blocker diminazene aceturate. These data provide evidence of the role of carbonic anhydrase and epithelial sodium channels in earthworm CO2 detection, establish that, similar to other subterranean-dwelling animals, earthworms are extremely tolerant of CO2, and contribute to our understanding of the mechanisms used by earthworms to detect and react to weak acids in their environment. Contribution to the field statementCarbon dioxide (CO2) is a major byproduct of cellular respiration and an important biological signal. The metabolism of animals living underground in burrows can cause the concentration of CO2 to increase above atmospheric CO2. Most animals have multiple molecular mechanisms that detect CO2 and find high concentrations aversive or noxious; some subterranean animals have adaptations that make them more tolerant of concentrated CO2. Earthworms live in burrows, are a keystone species for subterranean ecosystems, and in their lightless environment must rely primarily on tactile and chemical signals. Despite the profound importance of earthworms, few if any of the molecular mechanisms they use to detect these signals have been characterized. Here we use RNA sequencing to develop a list of candidate mechanisms that the European nightcrawler may use to respond to CO2. We also have developed an assay for comparing how noxious different concentrations of volatile compounds are to earthworms. In the present study, we utilize that assay with inhibitors to further narrow the possible multiple molecular mechanisms responsible for the detection of CO2. We suspect that our study is among the first attempts to combine RNA-sequencing technology and pharmacology to describe earthworm sensory biology.

physiology↗

Differential effects of redox conditions on the decomposition of litter and soil organic matter

Soil redox conditions exert substantial influence on biogeochemical processes in terrestrial ecosystems. Humid tropical forest soils are often characterized by fluctuating redox dynamics, yet how these dynamics affect patterns in soil versus litter decomposition and associated CO2 fluxes is not well understood. We used a 13C-labeled litter addition to explicitly follow the decomposition of litter-derived vs. native soil-derived organic matter in response to four different soil redox regimes--static oxic or anoxic, and two oscillating treatments--in soil from the Luquillo Experimental Forest, Puerto Rico. We coupled this incubation experiment with high-resolution mass spectrometry to characterize the preferential decomposition of specific classes of organic molecules. CO2 production from litter and soil organic matter (SOM) showed distinctly different responses to redox manipulation. The cumulative production of SOM-derived CO2 was positively correlated with the length of soil exposure to an oxic headspace (r = 0.89, n = 20), whereas cumulative 13C-litter-derived CO2 production was not linked to oxygen availability. The CO2 production rate from litter was highest under static anoxic conditions in the first half of the incubation period, and later dropped to the lowest among all redox treatments. In the consistently anoxic soils, we observed the depletion of more oxidized water-extractable organic matter (especially amino sugars, carbohydrates, and proteins) over time, suggesting that under anaerobic conditions, microbes preferentially used more oxidized litter-derived compounds during the early stages of decomposition. Results from kinetic modeling showed that more frequent anoxic exposure limited the decomposition of a slow-cycling C pool, but not a fast-cycling pool. Overall, our results demonstrate that substrate source--freshly added litter vs. native organic matter--plays an important role in the redox sensitivity of organic matter decomposition. In soil environments that regularly experience redox fluctuations, anaerobic heterotrophs can be surprisingly effective in degrading fresh plant litter.

ecology↗

Ecological and genomic attributes of novel bacterial taxa that thrive in subsurface soil horizons

While most bacterial and archaeal taxa living in surface soils remain undescribed, this problem is exacerbated in deeper soils owing to the unique oligotrophic conditions found in the subsurface. Additionally, previous studies of soil microbiomes have focused almost exclusively on surface soils, even though the microbes living in deeper soils also play critical roles in a wide range of biogeochemical processes. We examined soils collected from 20 distinct profiles across the U.S. to characterize the bacterial and archaeal communities that live in subsurface soils and to determine whether there are consistent changes in soil microbial communities with depth across a wide range of soil and environmental conditions. We found that bacterial and archaeal diversity generally decreased with depth, as did the degree of similarity of microbial communities to those found in surface horizons. We observed five phyla that consistently increased in relative abundance with depth across our soil profiles: Chloroflexi, Nitrospirae, Euryarchaeota, and candidate phyla GAL15 and Dormibacteraeota (formerly AD3). Leveraging the unusually high abundance of Dormibacteraeota at depth, we assembled genomes representative of this candidate phylum and identified traits that are likely to be beneficial in low nutrient environments, including the synthesis and storage of carbohydrates, the potential to use carbon monoxide (CO) as a supplemental energy source, and the ability to form spores. Together these attributes likely allow members of the candidate phylum Dormibacteraeota to flourish in deeper soils and provide insight into the survival and growth strategies employed by the microbes that thrive in oligotrophic soil environments.\n\nImportanceSoil profiles are rarely homogeneous. Resource availability and microbial abundances typically decrease with soil depth, but microbes found in deeper horizons are still important components of terrestrial ecosystems. By studying 20 soil profiles across the U.S., we documented consistent changes in soil bacterial and archaeal communities with depth. Deeper soils harbored distinct communities compared to the more commonly studied surface horizons. Most notably, we found that the candidate phylum Dormibacteraeota (formerly AD3) was often dominant in subsurface soils, and we used genomes from uncultivated members of this group to identify why these taxa are able to thrive in such resource-limited environments. Simply digging deeper into soil can reveal a surprising amount of novel microbes with unique adaptations to oligotrophic subsurface conditions.

microbiology↗

Redox fluctuations control the coupled cycling of iron and carbon in tropical forest soils

Oscillating redox conditions are the norm in tropical soils; driven by an ample supply of reductants, high moisture, microbial oxygen consumption, and finely textured clays that limit diffusion. Yet the net result of variable soil redox regimes on iron-organic matter (Fe-OM) associations in tropical soils owing to changing climate is poorly understood. Using a 44-day redox incubation experiment with humid tropical soils from Puerto Rico, we examined patterns of Fe and C transformation under four redox regimes: static anoxic, flux 4-day (4d oxic, 4d anoxic), flux 8-day (8d oxic, 4d anoxic) and static anoxic. Prolonged anoxia promoted reductive dissolution of Fe-oxides and an increase in short-range ordered (SRO) Fe oxides. Preferential dissolution of this less-crystalline Fe pool was evident immediately following a shift in bulk redox status (oxic to anoxic), and coincided with increased dissolved organic carbon, presumably due to acidification or direct release of OM from dissolving Fe(III) mineral phases. Average nominal oxidation state of water-soluble carbon was lowest under persistent anoxic conditions, suggesting more reduced OC is microbially preserved under reducing conditions. Anoxic soil compounds had high H/C values (similar to lignin-like metabolites) whereas oxic soil compounds had higher O/C values, akin to tannin- and cellulose-like components. Cumulative respiration derived from native soil organic carbon was highest in static oxic soils. These results highlight the volatility of mineral-OM interactions in tropical soils, and suggest that short-term impacts of shifting soil O2 availability control exchanges of C between mineral-sorbed and aqueous pools, implying that the periodicity of low-redox moments may control the fate of C in wet tropical soils.\n\nO_FIG O_LINKSMALLFIG WIDTH=200 HEIGHT=121 SRC=\"FIGDIR/small/312108_ufig1.gif\" ALT=\"Figure 1\">\nView larger version (23K):\norg.highwire.dtl.DTLVardef@add07borg.highwire.dtl.DTLVardef@15269bforg.highwire.dtl.DTLVardef@19ca034org.highwire.dtl.DTLVardef@1d9d793_HPS_FORMAT_FIGEXP M_FIG Toc Art C_FIG

ecology↗