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Coordinating environmental genomics and geochemistry reveals metabolic transitions in a hot spring ecosystem.

Swingley WD, Meyer-Dombard DR, Shock EL, Alsop EB, Falenski HD, Havig JR, Raymond J - PLoS ONE (2012)

Bottom Line: We improved automated annotation of the BP environmental genomes using BLAST-based Markov clustering.We show that changes in environmental conditions and energy availability are associated with dramatic shifts in microbial communities and metabolic function.The complementary analysis of biogeochemical and environmental genomic data from BP has allowed us to build ecosystem-based conceptual models for this hot spring, reconstructing whole metabolic networks in order to illuminate community roles in shaping and responding to geochemical variability.

View Article: PubMed Central - PubMed

Affiliation: School of Natural Sciences, University of California Merced, Merced, California, United States of America.

ABSTRACT
We have constructed a conceptual model of biogeochemical cycles and metabolic and microbial community shifts within a hot spring ecosystem via coordinated analysis of the "Bison Pool" (BP) Environmental Genome and a complementary contextual geochemical dataset of ~75 geochemical parameters. 2,321 16S rRNA clones and 470 megabases of environmental sequence data were produced from biofilms at five sites along the outflow of BP, an alkaline hot spring in Sentinel Meadow (Lower Geyser Basin) of Yellowstone National Park. This channel acts as a >22 m gradient of decreasing temperature, increasing dissolved oxygen, and changing availability of biologically important chemical species, such as those containing nitrogen and sulfur. Microbial life at BP transitions from a 92 °C chemotrophic streamer biofilm community in the BP source pool to a 56 °C phototrophic mat community. We improved automated annotation of the BP environmental genomes using BLAST-based Markov clustering. We have also assigned environmental genome sequences to individual microbial community members by complementing traditional homology-based assignment with nucleotide word-usage algorithms, allowing more than 70% of all reads to be assigned to source organisms. This assignment yields high genome coverage in dominant community members, facilitating reconstruction of nearly complete metabolic profiles and in-depth analysis of the relation between geochemical and metabolic changes along the outflow. We show that changes in environmental conditions and energy availability are associated with dramatic shifts in microbial communities and metabolic function. We have also identified an organism constituting a novel phylum in a metabolic "transition" community, located physically between the chemotroph- and phototroph-dominated sites. The complementary analysis of biogeochemical and environmental genomic data from BP has allowed us to build ecosystem-based conceptual models for this hot spring, reconstructing whole metabolic networks in order to illuminate community roles in shaping and responding to geochemical variability.

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Selected geochemical trends moving downstream at BP.Top and middle; chloride and oxygen isotope (of water) measurements, respectively, showing calculated evaporation trendlines imposed on the data; the slopes of the lines are set by the extent of evaporation required to account for the temperature decrease. Bottom; dissolved oxygen concentrations, representing redox processes in BP. All plots show chemosynthetic (far right), transition “fringe” (grey bar), and photosynthetic zones (far left).
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pone-0038108-g002: Selected geochemical trends moving downstream at BP.Top and middle; chloride and oxygen isotope (of water) measurements, respectively, showing calculated evaporation trendlines imposed on the data; the slopes of the lines are set by the extent of evaporation required to account for the temperature decrease. Bottom; dissolved oxygen concentrations, representing redox processes in BP. All plots show chemosynthetic (far right), transition “fringe” (grey bar), and photosynthetic zones (far left).

Mentions: The above description of the BP outflow represents the “typical” configuration during the summer months, when we are most apt to be sampling the hot spring. Atypical events, such as very heavy precipitation, have a dramatic affect on the flow of fluid in and around BP. We have observed substantial meadow “input” (organic-rich fluids and solids) in the source pool and entire outflow channel following an hour of steady, hard rainfall (Fig. S1k, l). This enrichment from the meadow brings a heretofore unquantified amount of carbon, nitrogen, and other nutrients into the system for several days. In addition, YNP has a short warm season of 2–3 months. The shallow cooling and mixing processes may be greatly enhanced in the colder months (September-June) when the air temperature may be >60°C colder than the summer months, and indeed our observations indicate that the photosynthetic fringe moves upstream in the winter [2]. Evidence of evaporation and redox processes are readily observed in the BP geochemical dataset (full dataset given in Table S1). Downstream values of δ18O and conservative ions such as Cl– (Figure 2) increase in accordance with the extent of evaporation required to account for the temperature decrease, while dissolved oxygen (DO) increases slightly up to site 3, likely as a result of atmospheric mixing, before a sharp increase proposed to be due to photosynthetic production of O2 at sites 4 and 5. Trace element concentrations in the outflow behave variably as physical and potentially biological parameters engage. For example, trace element concentrations typically rise through sites 1 and 2 due to probable evaporative effects (Figure 3). Between sites 3 and 5, where meadow influence and reduced stream flow affect the outflow channel, concentrations of measured trace elements may decrease due to dilution by meadow input or increase again with continued evaporation (e.g., W and Fe) (Figure 3). The four example trends given in Figure 3 (V, Mo, W, and Fe) are typical of trace elements measured, and concentrations appear to either follow a steady increase up to site 4, followed by a decrease at site 5 (as shown by V and Mo), or experience a sharp decrease in concentration at site 3 (as shown by Fe and W). In short, the physical and chemical nature of the outflow channel is regulated by expected processes, but may be highly variable over short distances and over time.


Coordinating environmental genomics and geochemistry reveals metabolic transitions in a hot spring ecosystem.

Swingley WD, Meyer-Dombard DR, Shock EL, Alsop EB, Falenski HD, Havig JR, Raymond J - PLoS ONE (2012)

Selected geochemical trends moving downstream at BP.Top and middle; chloride and oxygen isotope (of water) measurements, respectively, showing calculated evaporation trendlines imposed on the data; the slopes of the lines are set by the extent of evaporation required to account for the temperature decrease. Bottom; dissolved oxygen concentrations, representing redox processes in BP. All plots show chemosynthetic (far right), transition “fringe” (grey bar), and photosynthetic zones (far left).
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC3367023&req=5

pone-0038108-g002: Selected geochemical trends moving downstream at BP.Top and middle; chloride and oxygen isotope (of water) measurements, respectively, showing calculated evaporation trendlines imposed on the data; the slopes of the lines are set by the extent of evaporation required to account for the temperature decrease. Bottom; dissolved oxygen concentrations, representing redox processes in BP. All plots show chemosynthetic (far right), transition “fringe” (grey bar), and photosynthetic zones (far left).
Mentions: The above description of the BP outflow represents the “typical” configuration during the summer months, when we are most apt to be sampling the hot spring. Atypical events, such as very heavy precipitation, have a dramatic affect on the flow of fluid in and around BP. We have observed substantial meadow “input” (organic-rich fluids and solids) in the source pool and entire outflow channel following an hour of steady, hard rainfall (Fig. S1k, l). This enrichment from the meadow brings a heretofore unquantified amount of carbon, nitrogen, and other nutrients into the system for several days. In addition, YNP has a short warm season of 2–3 months. The shallow cooling and mixing processes may be greatly enhanced in the colder months (September-June) when the air temperature may be >60°C colder than the summer months, and indeed our observations indicate that the photosynthetic fringe moves upstream in the winter [2]. Evidence of evaporation and redox processes are readily observed in the BP geochemical dataset (full dataset given in Table S1). Downstream values of δ18O and conservative ions such as Cl– (Figure 2) increase in accordance with the extent of evaporation required to account for the temperature decrease, while dissolved oxygen (DO) increases slightly up to site 3, likely as a result of atmospheric mixing, before a sharp increase proposed to be due to photosynthetic production of O2 at sites 4 and 5. Trace element concentrations in the outflow behave variably as physical and potentially biological parameters engage. For example, trace element concentrations typically rise through sites 1 and 2 due to probable evaporative effects (Figure 3). Between sites 3 and 5, where meadow influence and reduced stream flow affect the outflow channel, concentrations of measured trace elements may decrease due to dilution by meadow input or increase again with continued evaporation (e.g., W and Fe) (Figure 3). The four example trends given in Figure 3 (V, Mo, W, and Fe) are typical of trace elements measured, and concentrations appear to either follow a steady increase up to site 4, followed by a decrease at site 5 (as shown by V and Mo), or experience a sharp decrease in concentration at site 3 (as shown by Fe and W). In short, the physical and chemical nature of the outflow channel is regulated by expected processes, but may be highly variable over short distances and over time.

Bottom Line: We improved automated annotation of the BP environmental genomes using BLAST-based Markov clustering.We show that changes in environmental conditions and energy availability are associated with dramatic shifts in microbial communities and metabolic function.The complementary analysis of biogeochemical and environmental genomic data from BP has allowed us to build ecosystem-based conceptual models for this hot spring, reconstructing whole metabolic networks in order to illuminate community roles in shaping and responding to geochemical variability.

View Article: PubMed Central - PubMed

Affiliation: School of Natural Sciences, University of California Merced, Merced, California, United States of America.

ABSTRACT
We have constructed a conceptual model of biogeochemical cycles and metabolic and microbial community shifts within a hot spring ecosystem via coordinated analysis of the "Bison Pool" (BP) Environmental Genome and a complementary contextual geochemical dataset of ~75 geochemical parameters. 2,321 16S rRNA clones and 470 megabases of environmental sequence data were produced from biofilms at five sites along the outflow of BP, an alkaline hot spring in Sentinel Meadow (Lower Geyser Basin) of Yellowstone National Park. This channel acts as a >22 m gradient of decreasing temperature, increasing dissolved oxygen, and changing availability of biologically important chemical species, such as those containing nitrogen and sulfur. Microbial life at BP transitions from a 92 °C chemotrophic streamer biofilm community in the BP source pool to a 56 °C phototrophic mat community. We improved automated annotation of the BP environmental genomes using BLAST-based Markov clustering. We have also assigned environmental genome sequences to individual microbial community members by complementing traditional homology-based assignment with nucleotide word-usage algorithms, allowing more than 70% of all reads to be assigned to source organisms. This assignment yields high genome coverage in dominant community members, facilitating reconstruction of nearly complete metabolic profiles and in-depth analysis of the relation between geochemical and metabolic changes along the outflow. We show that changes in environmental conditions and energy availability are associated with dramatic shifts in microbial communities and metabolic function. We have also identified an organism constituting a novel phylum in a metabolic "transition" community, located physically between the chemotroph- and phototroph-dominated sites. The complementary analysis of biogeochemical and environmental genomic data from BP has allowed us to build ecosystem-based conceptual models for this hot spring, reconstructing whole metabolic networks in order to illuminate community roles in shaping and responding to geochemical variability.

Show MeSH