Carbon and sulfur cycling below the chemocline in a meromictic lake and the identification of a novel taxonomic lineage in the FCB superphylum, Candidatus Aegiribacteria

Trinity L. Hamilton, Roderick J. Bovee, Sarah R. Sattin, Wiebke Mohr, William P. Gilhooly, Timothy W. Lyons, Ann Pearson, Jennifer L. Macalady

Research output: Contribution to journalArticle

5 Citations (Scopus)

Abstract

Mahoney Lake in British Columbia is an extreme meromictic system with unusually high levels of sulfate and sulfide present in the water column. As is common in strongly stratified lakes, Mahoney Lake hosts a dense, sulfide-oxidizing phototrophic microbial community where light reaches the chemocline. Below this "plate," the euxinic hypolimnion is anoxic, eutrophic, saline, and rich in sulfide, polysulfides, elemental sulfur, and other sulfur intermediates. While much is known regarding microbial communities in sunlit portions of euxinic systems, the composition and genetic potential of organisms living at aphotic depths have rarely been studied. Metagenomic sequencing of samples from the hypolimnion and the underlying sediments of Mahoney Lake indicate that multiple taxa contribute to sulfate reduction below the chemocline and that the hypolimnion and sediments each support distinct populations of sulfate reducing bacteria (SRB) that differ from the SRB populations observed in the chemocline. After assembling and binning the metagenomic datasets, we recovered near-complete genomes of dominant populations including two Deltaproteobacteria. One of the deltaproteobacterial genomes encoded a 16S rRNA sequence that was most closely related to the sulfur-disproportionating genus Dissulfuribacter and the other encoded a 16S rRNA sequence that was most closely related to the fatty acid- and aromatic acid-degrading genus Syntrophus. We also recovered two near-complete genomes of Firmicutes species. Analysis of concatenated ribosomal protein trees suggests these genomes are most closely related to extremely alkaliphilic genera Alkaliphilus and Dethiobacter. Our metagenomic data indicate that these Firmicutes contribute to carbon cycling below the chemocline. Lastly, we recovered a nearly complete genome from the sediment metagenome which represents a new genus within the FCB (Fibrobacteres, Chlorobi, Bacteroidetes) superphylum. Consistent with the geochemical data, we found little or no evidence for organisms capable of sulfide oxidation in the aphotic zone below the chemocline. Instead, comparison of functional genes below the chemocline are consistent with recovery of multiple populations capable of reducing oxidized sulfur. Our data support previous observations that at least some of the sulfide necessary to support the dense population of phototrophs in the chemocline is supplied from sulfate reduction in the hypolimnion and sediments. These studies provide key insights regarding the taxonomic and functional diversity within a euxinic environment and highlight the complexity of biogeochemical carbon and sulfur cycling necessary to maintain euxinia.

Original languageEnglish (US)
Article number598
JournalFrontiers in Microbiology
Volume7
Issue numberAPR
DOIs
StatePublished - Apr 27 2016

Fingerprint

Fibrobacteres
Chlorobi
Bacteroidetes
Sulfides
Lakes
Sulfur
Sulfates
Carbon
Metagenomics
Genome
Population
Deltaproteobacteria
Metagenome
Bacteria
British Columbia
Ribosomal Proteins
Fatty Acids
Light
Acids
Water

Keywords

  • Clostridia
  • DSR
  • Deltaproteobacteria
  • Euxinia
  • Meromictic
  • Sulfate
  • Sulfate reducing bacteria
  • Sulfide

Cite this

Carbon and sulfur cycling below the chemocline in a meromictic lake and the identification of a novel taxonomic lineage in the FCB superphylum, Candidatus Aegiribacteria. / Hamilton, Trinity L.; Bovee, Roderick J.; Sattin, Sarah R.; Mohr, Wiebke; Gilhooly, William P.; Lyons, Timothy W.; Pearson, Ann; Macalady, Jennifer L.

In: Frontiers in Microbiology, Vol. 7, No. APR, 598, 27.04.2016.

Research output: Contribution to journalArticle

Hamilton, Trinity L. ; Bovee, Roderick J. ; Sattin, Sarah R. ; Mohr, Wiebke ; Gilhooly, William P. ; Lyons, Timothy W. ; Pearson, Ann ; Macalady, Jennifer L. / Carbon and sulfur cycling below the chemocline in a meromictic lake and the identification of a novel taxonomic lineage in the FCB superphylum, Candidatus Aegiribacteria. In: Frontiers in Microbiology. 2016 ; Vol. 7, No. APR.
@article{d9f80ac9cf2942e594f4bce3b98dd3f8,
title = "Carbon and sulfur cycling below the chemocline in a meromictic lake and the identification of a novel taxonomic lineage in the FCB superphylum, Candidatus Aegiribacteria",
abstract = "Mahoney Lake in British Columbia is an extreme meromictic system with unusually high levels of sulfate and sulfide present in the water column. As is common in strongly stratified lakes, Mahoney Lake hosts a dense, sulfide-oxidizing phototrophic microbial community where light reaches the chemocline. Below this {"}plate,{"} the euxinic hypolimnion is anoxic, eutrophic, saline, and rich in sulfide, polysulfides, elemental sulfur, and other sulfur intermediates. While much is known regarding microbial communities in sunlit portions of euxinic systems, the composition and genetic potential of organisms living at aphotic depths have rarely been studied. Metagenomic sequencing of samples from the hypolimnion and the underlying sediments of Mahoney Lake indicate that multiple taxa contribute to sulfate reduction below the chemocline and that the hypolimnion and sediments each support distinct populations of sulfate reducing bacteria (SRB) that differ from the SRB populations observed in the chemocline. After assembling and binning the metagenomic datasets, we recovered near-complete genomes of dominant populations including two Deltaproteobacteria. One of the deltaproteobacterial genomes encoded a 16S rRNA sequence that was most closely related to the sulfur-disproportionating genus Dissulfuribacter and the other encoded a 16S rRNA sequence that was most closely related to the fatty acid- and aromatic acid-degrading genus Syntrophus. We also recovered two near-complete genomes of Firmicutes species. Analysis of concatenated ribosomal protein trees suggests these genomes are most closely related to extremely alkaliphilic genera Alkaliphilus and Dethiobacter. Our metagenomic data indicate that these Firmicutes contribute to carbon cycling below the chemocline. Lastly, we recovered a nearly complete genome from the sediment metagenome which represents a new genus within the FCB (Fibrobacteres, Chlorobi, Bacteroidetes) superphylum. Consistent with the geochemical data, we found little or no evidence for organisms capable of sulfide oxidation in the aphotic zone below the chemocline. Instead, comparison of functional genes below the chemocline are consistent with recovery of multiple populations capable of reducing oxidized sulfur. Our data support previous observations that at least some of the sulfide necessary to support the dense population of phototrophs in the chemocline is supplied from sulfate reduction in the hypolimnion and sediments. These studies provide key insights regarding the taxonomic and functional diversity within a euxinic environment and highlight the complexity of biogeochemical carbon and sulfur cycling necessary to maintain euxinia.",
keywords = "Clostridia, DSR, Deltaproteobacteria, Euxinia, Meromictic, Sulfate, Sulfate reducing bacteria, Sulfide",
author = "Hamilton, {Trinity L.} and Bovee, {Roderick J.} and Sattin, {Sarah R.} and Wiebke Mohr and Gilhooly, {William P.} and Lyons, {Timothy W.} and Ann Pearson and Macalady, {Jennifer L.}",
year = "2016",
month = "4",
day = "27",
doi = "10.3389/fmicb.2016.00598",
language = "English (US)",
volume = "7",
journal = "Frontiers in Microbiology",
issn = "1664-302X",
publisher = "Frontiers Media S. A.",
number = "APR",

}

TY - JOUR

T1 - Carbon and sulfur cycling below the chemocline in a meromictic lake and the identification of a novel taxonomic lineage in the FCB superphylum, Candidatus Aegiribacteria

AU - Hamilton, Trinity L.

AU - Bovee, Roderick J.

AU - Sattin, Sarah R.

AU - Mohr, Wiebke

AU - Gilhooly, William P.

AU - Lyons, Timothy W.

AU - Pearson, Ann

AU - Macalady, Jennifer L.

PY - 2016/4/27

Y1 - 2016/4/27

N2 - Mahoney Lake in British Columbia is an extreme meromictic system with unusually high levels of sulfate and sulfide present in the water column. As is common in strongly stratified lakes, Mahoney Lake hosts a dense, sulfide-oxidizing phototrophic microbial community where light reaches the chemocline. Below this "plate," the euxinic hypolimnion is anoxic, eutrophic, saline, and rich in sulfide, polysulfides, elemental sulfur, and other sulfur intermediates. While much is known regarding microbial communities in sunlit portions of euxinic systems, the composition and genetic potential of organisms living at aphotic depths have rarely been studied. Metagenomic sequencing of samples from the hypolimnion and the underlying sediments of Mahoney Lake indicate that multiple taxa contribute to sulfate reduction below the chemocline and that the hypolimnion and sediments each support distinct populations of sulfate reducing bacteria (SRB) that differ from the SRB populations observed in the chemocline. After assembling and binning the metagenomic datasets, we recovered near-complete genomes of dominant populations including two Deltaproteobacteria. One of the deltaproteobacterial genomes encoded a 16S rRNA sequence that was most closely related to the sulfur-disproportionating genus Dissulfuribacter and the other encoded a 16S rRNA sequence that was most closely related to the fatty acid- and aromatic acid-degrading genus Syntrophus. We also recovered two near-complete genomes of Firmicutes species. Analysis of concatenated ribosomal protein trees suggests these genomes are most closely related to extremely alkaliphilic genera Alkaliphilus and Dethiobacter. Our metagenomic data indicate that these Firmicutes contribute to carbon cycling below the chemocline. Lastly, we recovered a nearly complete genome from the sediment metagenome which represents a new genus within the FCB (Fibrobacteres, Chlorobi, Bacteroidetes) superphylum. Consistent with the geochemical data, we found little or no evidence for organisms capable of sulfide oxidation in the aphotic zone below the chemocline. Instead, comparison of functional genes below the chemocline are consistent with recovery of multiple populations capable of reducing oxidized sulfur. Our data support previous observations that at least some of the sulfide necessary to support the dense population of phototrophs in the chemocline is supplied from sulfate reduction in the hypolimnion and sediments. These studies provide key insights regarding the taxonomic and functional diversity within a euxinic environment and highlight the complexity of biogeochemical carbon and sulfur cycling necessary to maintain euxinia.

AB - Mahoney Lake in British Columbia is an extreme meromictic system with unusually high levels of sulfate and sulfide present in the water column. As is common in strongly stratified lakes, Mahoney Lake hosts a dense, sulfide-oxidizing phototrophic microbial community where light reaches the chemocline. Below this "plate," the euxinic hypolimnion is anoxic, eutrophic, saline, and rich in sulfide, polysulfides, elemental sulfur, and other sulfur intermediates. While much is known regarding microbial communities in sunlit portions of euxinic systems, the composition and genetic potential of organisms living at aphotic depths have rarely been studied. Metagenomic sequencing of samples from the hypolimnion and the underlying sediments of Mahoney Lake indicate that multiple taxa contribute to sulfate reduction below the chemocline and that the hypolimnion and sediments each support distinct populations of sulfate reducing bacteria (SRB) that differ from the SRB populations observed in the chemocline. After assembling and binning the metagenomic datasets, we recovered near-complete genomes of dominant populations including two Deltaproteobacteria. One of the deltaproteobacterial genomes encoded a 16S rRNA sequence that was most closely related to the sulfur-disproportionating genus Dissulfuribacter and the other encoded a 16S rRNA sequence that was most closely related to the fatty acid- and aromatic acid-degrading genus Syntrophus. We also recovered two near-complete genomes of Firmicutes species. Analysis of concatenated ribosomal protein trees suggests these genomes are most closely related to extremely alkaliphilic genera Alkaliphilus and Dethiobacter. Our metagenomic data indicate that these Firmicutes contribute to carbon cycling below the chemocline. Lastly, we recovered a nearly complete genome from the sediment metagenome which represents a new genus within the FCB (Fibrobacteres, Chlorobi, Bacteroidetes) superphylum. Consistent with the geochemical data, we found little or no evidence for organisms capable of sulfide oxidation in the aphotic zone below the chemocline. Instead, comparison of functional genes below the chemocline are consistent with recovery of multiple populations capable of reducing oxidized sulfur. Our data support previous observations that at least some of the sulfide necessary to support the dense population of phototrophs in the chemocline is supplied from sulfate reduction in the hypolimnion and sediments. These studies provide key insights regarding the taxonomic and functional diversity within a euxinic environment and highlight the complexity of biogeochemical carbon and sulfur cycling necessary to maintain euxinia.

KW - Clostridia

KW - DSR

KW - Deltaproteobacteria

KW - Euxinia

KW - Meromictic

KW - Sulfate

KW - Sulfate reducing bacteria

KW - Sulfide

UR - http://www.scopus.com/inward/record.url?scp=84966333714&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=84966333714&partnerID=8YFLogxK

U2 - 10.3389/fmicb.2016.00598

DO - 10.3389/fmicb.2016.00598

M3 - Article

VL - 7

JO - Frontiers in Microbiology

JF - Frontiers in Microbiology

SN - 1664-302X

IS - APR

M1 - 598

ER -