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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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Map of BP, showing the five sample locations used in this study.Modified from Havig et al. (2011) and originally drafted by G.R. Osburn.
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pone-0038108-g001: Map of BP, showing the five sample locations used in this study.Modified from Havig et al. (2011) and originally drafted by G.R. Osburn.

Mentions: Samples of biofilm were collected on July 19, 2005 at “Bison Pool” (Thermal Inventory Number LSMG 013) with sterile implements from the main pool and four locations along the BP outflow, and named as sites 1–5, from source to bottom of the outflow. A map of BP at the time of sampling is shown in Figure 1, and images are found in Figure S1. Additional analyses and description of the BP location can be found in Meyer-Dombard et al. [4], Havig et al. [2] and Dick & Shock [1]. The five samples analyzed here consist of native Streamer Biofilm Communities (e.g. SBCs, [4]) at sites 1–3, and stratified photosynthetic mats at sites 4 and 5. Detailed photographs of each of the five collected biofilms are given in Havig et al. [2], and a few are available in Figure S1b, and S1c. SBC samples, which typically lay <1 cm below the water-air interface, were collected with forceps. Photosynthetic mats were sampled vertically from the surface of the mat down to the sediment interface, avoiding sediment particles as possible, and homogenized (individual layers of the mat were not separately analyzed). Photosynthetic mats were typically <0.5 cm thick, and the top most layers were a few mm below the water-air interface. Samples were placed in sterile vials on ice for several hours while in the field, and were frozen immediately on return to our field laboratory. Samples for geochemical analysis of spring fluids were specifically collected at each of the above sites 1–5 to coordinate with the samples destined for genomic analysis. Fluids were collected in the flowing portion of the runoff channel above the sediment interface (i.e. not pore fluids). Samples for analysis of trace elements, major ions, and redox sensitive species were collected, in accordance with previous methods [29], [30]. Measurements made in the field were done in replicate when possible, and we have previously estimated an uncertainty of ∼10%; IC and ICP-MS analyses are done in replicate and typical uncertainties are <1% [28]. Sample collection for field studies was carried out under National Park Service permit YELL-05434.


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)

Map of BP, showing the five sample locations used in this study.Modified from Havig et al. (2011) and originally drafted by G.R. Osburn.
© Copyright Policy
Related In: Results  -  Collection

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

pone-0038108-g001: Map of BP, showing the five sample locations used in this study.Modified from Havig et al. (2011) and originally drafted by G.R. Osburn.
Mentions: Samples of biofilm were collected on July 19, 2005 at “Bison Pool” (Thermal Inventory Number LSMG 013) with sterile implements from the main pool and four locations along the BP outflow, and named as sites 1–5, from source to bottom of the outflow. A map of BP at the time of sampling is shown in Figure 1, and images are found in Figure S1. Additional analyses and description of the BP location can be found in Meyer-Dombard et al. [4], Havig et al. [2] and Dick & Shock [1]. The five samples analyzed here consist of native Streamer Biofilm Communities (e.g. SBCs, [4]) at sites 1–3, and stratified photosynthetic mats at sites 4 and 5. Detailed photographs of each of the five collected biofilms are given in Havig et al. [2], and a few are available in Figure S1b, and S1c. SBC samples, which typically lay <1 cm below the water-air interface, were collected with forceps. Photosynthetic mats were sampled vertically from the surface of the mat down to the sediment interface, avoiding sediment particles as possible, and homogenized (individual layers of the mat were not separately analyzed). Photosynthetic mats were typically <0.5 cm thick, and the top most layers were a few mm below the water-air interface. Samples were placed in sterile vials on ice for several hours while in the field, and were frozen immediately on return to our field laboratory. Samples for geochemical analysis of spring fluids were specifically collected at each of the above sites 1–5 to coordinate with the samples destined for genomic analysis. Fluids were collected in the flowing portion of the runoff channel above the sediment interface (i.e. not pore fluids). Samples for analysis of trace elements, major ions, and redox sensitive species were collected, in accordance with previous methods [29], [30]. Measurements made in the field were done in replicate when possible, and we have previously estimated an uncertainty of ∼10%; IC and ICP-MS analyses are done in replicate and typical uncertainties are <1% [28]. Sample collection for field studies was carried out under National Park Service permit YELL-05434.

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