Comparative genomics in acid mine drainage biofilm communities reveals metabolic and structural differentiation of co-occurring archaea
Background Metal sulfide mineral dissolution during bioleaching and acid mine drainage (AMD) formation creates an environment that is inhospitable to most life. Despite dominance by a small number of bacteria, AMD microbial biofilm communities contain a notable variety of coexisting and closely rel...
| Main Authors: | , , , , , , |
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| Format: | Article |
| Language: | English |
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BioMed Central
2016
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| Online Access: | http://hdl.handle.net/1721.1/101196 https://orcid.org/0000-0002-7616-551X |
| _version_ | 1826216812137676800 |
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| author | Castelle, Cindy Yelton, Alexis P. Comolli, Luis R. Justice, Nicholas B. Denef, Vincent J. Thomas, Brian C. Banfield, Jillian F. |
| author2 | Massachusetts Institute of Technology. Department of Civil and Environmental Engineering |
| author_facet | Massachusetts Institute of Technology. Department of Civil and Environmental Engineering Castelle, Cindy Yelton, Alexis P. Comolli, Luis R. Justice, Nicholas B. Denef, Vincent J. Thomas, Brian C. Banfield, Jillian F. |
| author_sort | Castelle, Cindy |
| collection | MIT |
| description | Background
Metal sulfide mineral dissolution during bioleaching and acid mine drainage (AMD) formation creates an environment that is inhospitable to most life. Despite dominance by a small number of bacteria, AMD microbial biofilm communities contain a notable variety of coexisting and closely related Euryarchaea, most of which have defied cultivation efforts. For this reason, we used metagenomics to analyze variation in gene content that may contribute to niche differentiation among co-occurring AMD archaea. Our analyses targeted members of the Thermoplasmatales and related archaea. These results greatly expand genomic information available for this archaeal order.
Results
We reconstructed near-complete genomes for uncultivated, relatively low abundance organisms A-, E-, and Gplasma, members of Thermoplasmatales order, and for a novel organism, Iplasma. Genomic analyses of these organisms, as well as Ferroplasma type I and II, reveal that all are facultative aerobic heterotrophs with the ability to use many of the same carbon substrates, including methanol. Most of the genomes share genes for toxic metal resistance and surface-layer production. Only Aplasma and Eplasma have a full suite of flagellar genes whereas all but the Ferroplasma spp. have genes for pili production. Cryogenic-electron microscopy (cryo-EM) and tomography (cryo-ET) strengthen these metagenomics-based ultrastructural predictions. Notably, only Aplasma, Gplasma and the Ferroplasma spp. have predicted iron oxidation genes and Eplasma and Iplasma lack most genes for cobalamin, valine, (iso)leucine and histidine synthesis.
Conclusion
The Thermoplasmatales AMD archaea share a large number of metabolic capabilities. All of the uncultivated organisms studied here (A-, E-, G-, and Iplasma) are metabolically very similar to characterized Ferroplasma spp., differentiating themselves mainly in their genetic capabilities for biosynthesis, motility, and possibly iron oxidation. These results indicate that subtle, but important genomic differences, coupled with unknown differences in gene expression, distinguish these organisms enough to allow for co-existence. Overall this study reveals shared features of organisms from the Thermoplasmatales lineage and provides new insights into the functioning of AMD communities. |
| first_indexed | 2024-09-23T16:53:30Z |
| format | Article |
| id | mit-1721.1/101196 |
| institution | Massachusetts Institute of Technology |
| language | English |
| last_indexed | 2024-09-23T16:53:30Z |
| publishDate | 2016 |
| publisher | BioMed Central |
| record_format | dspace |
| spelling | mit-1721.1/1011962022-09-29T22:14:35Z Comparative genomics in acid mine drainage biofilm communities reveals metabolic and structural differentiation of co-occurring archaea Castelle, Cindy Yelton, Alexis P. Comolli, Luis R. Justice, Nicholas B. Denef, Vincent J. Thomas, Brian C. Banfield, Jillian F. Massachusetts Institute of Technology. Department of Civil and Environmental Engineering Yelton, Alexis P. Background Metal sulfide mineral dissolution during bioleaching and acid mine drainage (AMD) formation creates an environment that is inhospitable to most life. Despite dominance by a small number of bacteria, AMD microbial biofilm communities contain a notable variety of coexisting and closely related Euryarchaea, most of which have defied cultivation efforts. For this reason, we used metagenomics to analyze variation in gene content that may contribute to niche differentiation among co-occurring AMD archaea. Our analyses targeted members of the Thermoplasmatales and related archaea. These results greatly expand genomic information available for this archaeal order. Results We reconstructed near-complete genomes for uncultivated, relatively low abundance organisms A-, E-, and Gplasma, members of Thermoplasmatales order, and for a novel organism, Iplasma. Genomic analyses of these organisms, as well as Ferroplasma type I and II, reveal that all are facultative aerobic heterotrophs with the ability to use many of the same carbon substrates, including methanol. Most of the genomes share genes for toxic metal resistance and surface-layer production. Only Aplasma and Eplasma have a full suite of flagellar genes whereas all but the Ferroplasma spp. have genes for pili production. Cryogenic-electron microscopy (cryo-EM) and tomography (cryo-ET) strengthen these metagenomics-based ultrastructural predictions. Notably, only Aplasma, Gplasma and the Ferroplasma spp. have predicted iron oxidation genes and Eplasma and Iplasma lack most genes for cobalamin, valine, (iso)leucine and histidine synthesis. Conclusion The Thermoplasmatales AMD archaea share a large number of metabolic capabilities. All of the uncultivated organisms studied here (A-, E-, G-, and Iplasma) are metabolically very similar to characterized Ferroplasma spp., differentiating themselves mainly in their genetic capabilities for biosynthesis, motility, and possibly iron oxidation. These results indicate that subtle, but important genomic differences, coupled with unknown differences in gene expression, distinguish these organisms enough to allow for co-existence. Overall this study reveals shared features of organisms from the Thermoplasmatales lineage and provides new insights into the functioning of AMD communities. United States. Dept. of Energy. Genomics:GTL (Grant DE-FG02-05ER64134) National Science Foundation (U.S.). Graduate Research Fellowship 2016-02-17T15:15:16Z 2016-02-17T15:15:16Z 2013-07 2013-02 2016-02-16T05:29:15Z Article http://purl.org/eprint/type/JournalArticle 1471-2164 http://hdl.handle.net/1721.1/101196 Yelton, Alexis P, Luis R Comolli, Nicholas B Justice, Cindy Castelle, Vincent J Denef, Brian C Thomas, and Jillian F Banfield. “Comparative Genomics in Acid Mine Drainage Biofilm Communities Reveals Metabolic and Structural Differentiation of Co-Occurring Archaea.” BMC Genomics 14, no. 1 (2013): 485. https://orcid.org/0000-0002-7616-551X en http://dx.doi.org/10.1186/1471-2164-14-485 BMC Genomics Creative Commons Attribution http://creativecommons.org/licenses/by/2.0/ Yelton et al.; licensee BioMed Central Ltd. application/pdf BioMed Central BioMed Central |
| spellingShingle | Castelle, Cindy Yelton, Alexis P. Comolli, Luis R. Justice, Nicholas B. Denef, Vincent J. Thomas, Brian C. Banfield, Jillian F. Comparative genomics in acid mine drainage biofilm communities reveals metabolic and structural differentiation of co-occurring archaea |
| title | Comparative genomics in acid mine drainage biofilm communities reveals metabolic and structural differentiation of co-occurring archaea |
| title_full | Comparative genomics in acid mine drainage biofilm communities reveals metabolic and structural differentiation of co-occurring archaea |
| title_fullStr | Comparative genomics in acid mine drainage biofilm communities reveals metabolic and structural differentiation of co-occurring archaea |
| title_full_unstemmed | Comparative genomics in acid mine drainage biofilm communities reveals metabolic and structural differentiation of co-occurring archaea |
| title_short | Comparative genomics in acid mine drainage biofilm communities reveals metabolic and structural differentiation of co-occurring archaea |
| title_sort | comparative genomics in acid mine drainage biofilm communities reveals metabolic and structural differentiation of co occurring archaea |
| url | http://hdl.handle.net/1721.1/101196 https://orcid.org/0000-0002-7616-551X |
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