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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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Nitrogen cycle in BP.Top plot; concentrations of nitrate (solid circles) and nitrite (open circles) as a function of downstream flow. Plot shows chemosynthetic (far right), transition “fringe” (grey bar), and phostosynthetic zones (far left). Bottom histogram shows total counts of genes associated with denitrification (black bars), N2-fixation (grey bars), and nitrification (diagonal filled bars) normalized to the smallest total dataset. Denitrification genes included nitrate reductase (nar), nitrite reductase (nir), nitric oxide reductase (nor), and nitrous oxide reductase (nos). N2-fixation was counted by nitrogenase (nif), and nitrification genes included hydroxylamine oxidase hao and ammonia monooxygenase (amo, which was not found in any sample).
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pone-0038108-g007: Nitrogen cycle in BP.Top plot; concentrations of nitrate (solid circles) and nitrite (open circles) as a function of downstream flow. Plot shows chemosynthetic (far right), transition “fringe” (grey bar), and phostosynthetic zones (far left). Bottom histogram shows total counts of genes associated with denitrification (black bars), N2-fixation (grey bars), and nitrification (diagonal filled bars) normalized to the smallest total dataset. Denitrification genes included nitrate reductase (nar), nitrite reductase (nir), nitric oxide reductase (nor), and nitrous oxide reductase (nos). N2-fixation was counted by nitrogenase (nif), and nitrification genes included hydroxylamine oxidase hao and ammonia monooxygenase (amo, which was not found in any sample).

Mentions: Concentrations of NO3− and NO2− at the time samples were taken for the BPEG analysis are shown in Figure 7. Nitrate concentrations decrease from 0.045 mM at sites 1 and 2 to 0.035 mM at the site 3 transitional fringe environment before increasing again in the photosynthetic zone. Simultaneously, NO2− increases from ∼0.3 µM to ∼0.5 µM. Ammonia is below detection limits in BP fluids using the spectrophotometric methods described. While not all the nitrogen as NO3− lost is accounted for as NO2−, these data may indicate microbial reduction of NO3− in the outflow channel.


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)

Nitrogen cycle in BP.Top plot; concentrations of nitrate (solid circles) and nitrite (open circles) as a function of downstream flow. Plot shows chemosynthetic (far right), transition “fringe” (grey bar), and phostosynthetic zones (far left). Bottom histogram shows total counts of genes associated with denitrification (black bars), N2-fixation (grey bars), and nitrification (diagonal filled bars) normalized to the smallest total dataset. Denitrification genes included nitrate reductase (nar), nitrite reductase (nir), nitric oxide reductase (nor), and nitrous oxide reductase (nos). N2-fixation was counted by nitrogenase (nif), and nitrification genes included hydroxylamine oxidase hao and ammonia monooxygenase (amo, which was not found in any sample).
© Copyright Policy
Related In: Results  -  Collection

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

pone-0038108-g007: Nitrogen cycle in BP.Top plot; concentrations of nitrate (solid circles) and nitrite (open circles) as a function of downstream flow. Plot shows chemosynthetic (far right), transition “fringe” (grey bar), and phostosynthetic zones (far left). Bottom histogram shows total counts of genes associated with denitrification (black bars), N2-fixation (grey bars), and nitrification (diagonal filled bars) normalized to the smallest total dataset. Denitrification genes included nitrate reductase (nar), nitrite reductase (nir), nitric oxide reductase (nor), and nitrous oxide reductase (nos). N2-fixation was counted by nitrogenase (nif), and nitrification genes included hydroxylamine oxidase hao and ammonia monooxygenase (amo, which was not found in any sample).
Mentions: Concentrations of NO3− and NO2− at the time samples were taken for the BPEG analysis are shown in Figure 7. Nitrate concentrations decrease from 0.045 mM at sites 1 and 2 to 0.035 mM at the site 3 transitional fringe environment before increasing again in the photosynthetic zone. Simultaneously, NO2− increases from ∼0.3 µM to ∼0.5 µM. Ammonia is below detection limits in BP fluids using the spectrophotometric methods described. While not all the nitrogen as NO3− lost is accounted for as NO2−, these data may indicate microbial reduction of NO3− in the outflow channel.

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