Coupled reductive and oxidative sulfur cycling in the phototrophic plate of a meromictic lake
Mahoney Lake represents an extreme meromictic model system and is a valuable site for examining the organisms and processes that sustain photic zone euxinia (PZE). A single population of purple sulfur bacteria (PSB) living in a dense phototrophic plate in the chemocline is responsible for most of th...
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| Published in: | Geobiology Vol. 12; no. 5; pp. 451 - 468 |
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| Main Authors: | , , , , , , , , , , , , , , |
| Format: | Journal Article |
| Language: | English |
| Published: |
England
Blackwell Publishing Ltd
01-09-2014
Wiley Subscription Services, Inc |
| Subjects: | |
| Online Access: | Get full text |
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| Summary: | Mahoney Lake represents an extreme meromictic model system and is a valuable site for examining the organisms and processes that sustain photic zone euxinia (PZE). A single population of purple sulfur bacteria (PSB) living in a dense phototrophic plate in the chemocline is responsible for most of the primary production in Mahoney Lake. Here, we present metagenomic data from this phototrophic plate – including the genome of the major PSB, as obtained from both a highly enriched culture and from the metagenomic data – as well as evidence for multiple other taxa that contribute to the oxidative sulfur cycle and to sulfate reduction. The planktonic PSB is a member of the Chromatiaceae, here renamed Thiohalocapsa sp. strain ML1. It produces the carotenoid okenone, yet its closest relatives are benthic PSB isolates, a finding that may complicate the use of okenone (okenane) as a biomarker for ancient PZE. Favorable thermodynamics for non‐phototrophic sulfide oxidation and sulfate reduction reactions also occur in the plate, and a suite of organisms capable of oxidizing and reducing sulfur is apparent in the metagenome. Fluctuating supplies of both reduced carbon and reduced sulfur to the chemocline may partly account for the diversity of both autotrophic and heterotrophic species. Collectively, the data demonstrate the physiological potential for maintaining complex sulfur and carbon cycles in an anoxic water column, driven by the input of exogenous organic matter. This is consistent with suggestions that high levels of oxygenic primary production maintain episodes of PZE in Earth's history and that such communities should support a diversity of sulfur cycle reactions. |
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| Bibliography: | the NAI Postdoctoral Program NASA Exobiology Program Data S1 Supplementary methods and results. Table S1 Metagenome summary statistics. Table S2 Marker genes used to evaluate genome completion of the isolate genome, strain ML1, and the ML-Gamma and ML-Epsilon genomic bins. Table S3 Marker genes used to evaluate genome completion of the Deltaproteobacteria community genome bins. Table S4 Orthologous group markers and their abundance used to estimate the number of complete genomes in the Deltaproteobacteria community genome bins. Table S5 Single-copy phylogenetic marker genes used for taxonomic assignment of the ML-Gamma and the ML-Epsilon genomic bins. Table S6 List of genes from the Mahoney Lake 7-m metagenome identified and included in functional gene phylogenetic analyses. Table S7 Number and taxonomic affiliation of key genes involved in the sulfur cycle. Table S8 Accession numbers of the Sqr sequences included in Fig. S6. Table S9 Summary of community genomic bins of Deltaproteobacteria spp. Table S10 Calculations for ΔG = ΔG0 + RTlnQ at 18°C for selected sulfur redox reactions in situ. Table S11 List of organisms from which NifH/VnfH/AnfH were identified and included in the phylogenetic analysis of NifH/VnfH/AnfH identified in from the Mahoney Lake 7-m metagenome. Fig. S1 ESOM (repeating-tiled view) bins of the tetranucleotide frequency signatures of the 7-m metagenome with bins of interest indicated. Fig. S2 The estimated number of SRB genomes recovered from the Mahoney Lake metagenome. Fig. S3 Maximum likelihood phylogenetic tree of 19 concatenated single-copy ribosomal proteins showing the placement of the strain ML1 and ML-Gamma compared to closely related Gammaproteobacteria spp. for which genome sequences are available. Fig. S4 Phylogenetic diversity of RuBisCO in the Mahoney Lake chemocline. Maximum likelihood phylogenetic trees constructed from CbbL and CbbM sequences mined from the ML 7-m metagenome and the NCBI and IMG/M database. Fig. S5 Phylogenetic diversity of the nitrogenase Fe protein in the Mahoney Lake chemocline. Fig. S6 Maximum likelihood phylogenetic tree of translated genes sequences encoding okenone C-4/4' ketolase (CruO), okenone accessory ketolase (CruS), carotenoid desaturase (CrtD) and methoxyneurosporine dehydrogenases (CrtD/CrtI family homologs). Fig. S7 Maximum likelihood phylogenetic tree of Sqr. Sequences were mined from the 7-m metagenome (Table S6) and the NCBI and IMG/M database. Fig. S8 Taxonomic diversity of SRB-affiliated SP3 proteins and the Predicted role of the ML SRB spp. in the sulfur cycle. Fig. S9 Phylogenetic diversity of RuBisCO in the Mahoney Lake chemocline. Maximum likelihood phylogenetic trees constructed from CbbL and CbbM sequences mined from the ML 7-m metagenome and the NCBI and IMG/M database. Fig. S10 Calculated values for ΔG = ΔG0 + RTlnQ at 18 °C for selected sulfur redox reactions in situ, at depths above, within, and below the purple chemocline. Gordon and Betty Moore Foundation ark:/67375/WNG-4FZHNQH0-4 istex:92271473CDC0B8E5F5AB057B2041BEB329F9043B Marie Curie International Outgoing Fellowship within the 7th European Community Framework Programme National Science Foundation - No. NSF EAR-0525503; No. MCB-0523100; No. NNX09AM87G ArticleID:GBI12092 ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 |
| ISSN: | 1472-4677 1472-4669 |
| DOI: | 10.1111/gbi.12092 |