Small and mighty: adaptation of superphylum Patescibacteria to groundwater environment drives their genome simplicity
Background: The newly defined superphylum Patescibacteria such as Parcubacteria (OD1) and Microgenomates (OP11) has been found to be prevalent in groundwater, sediment, lake, and other aquifer environments. Recently increasing attention has been paid to this diverse superphylum including > 20 can...
| Main Authors: | , , , , , , , , , , , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
| Published: |
Springer Science and Business Media LLC
2020
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| Online Access: | https://hdl.handle.net/1721.1/128881 |
| _version_ | 1826202514608881664 |
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| author | Tian, Renmao Ning, Daliang He, Zhili Zhang, Ping Spencer, Sarah J. Gao, Shuhong Shi, Weiling Wu, Linwei Zhang, Ya Yang, Yunfeng Adams, Benjamin G. Rocha, Andrea M. Detienne, Brittny L. Lowe, Kenneth A. Joyner, Dominique C. Klingeman, Dawn M. Arkin, Adam P. Fields, Matthew W. Hazen, Terry C. Stahl, David A. Alm, Eric J Zhou, Jizhong |
| author2 | Massachusetts Institute of Technology. Department of Biological Engineering |
| author_facet | Massachusetts Institute of Technology. Department of Biological Engineering Tian, Renmao Ning, Daliang He, Zhili Zhang, Ping Spencer, Sarah J. Gao, Shuhong Shi, Weiling Wu, Linwei Zhang, Ya Yang, Yunfeng Adams, Benjamin G. Rocha, Andrea M. Detienne, Brittny L. Lowe, Kenneth A. Joyner, Dominique C. Klingeman, Dawn M. Arkin, Adam P. Fields, Matthew W. Hazen, Terry C. Stahl, David A. Alm, Eric J Zhou, Jizhong |
| author_sort | Tian, Renmao |
| collection | MIT |
| description | Background: The newly defined superphylum Patescibacteria such as Parcubacteria (OD1) and Microgenomates (OP11) has been found to be prevalent in groundwater, sediment, lake, and other aquifer environments. Recently increasing attention has been paid to this diverse superphylum including > 20 candidate phyla (a large part of the candidate phylum radiation, CPR) because it refreshed our view of the tree of life. However, adaptive traits contributing to its prevalence are still not well known. Results: Here, we investigated the genomic features and metabolic pathways of Patescibacteria in groundwater through genome-resolved metagenomics analysis of > 600 Gbp sequence data. We observed that, while the members of Patescibacteria have reduced genomes (~ 1 Mbp) exclusively, functions essential to growth and reproduction such as genetic information processing were retained. Surprisingly, they have sharply reduced redundant and nonessential functions, including specific metabolic activities and stress response systems. The Patescibacteria have ultra-small cells and simplified membrane structures, including flagellar assembly, transporters, and two-component systems. Despite the lack of CRISPR viral defense, the bacteria may evade predation through deletion of common membrane phage receptors and other alternative strategies, which may explain the low representation of prophage proteins in their genomes and lack of CRISPR. By establishing the linkages between bacterial features and the groundwater environmental conditions, our results provide important insights into the functions and evolution of this CPR group. Conclusions: We found that Patescibacteria has streamlined many functions while acquiring advantages such as avoiding phage invasion, to adapt to the groundwater environment. The unique features of small genome size, ultra-small cell size, and lacking CRISPR of this large lineage are bringing new understandings on life of Bacteria. Our results provide important insights into the mechanisms for adaptation of the superphylum in the groundwater environments, and demonstrate a case where less is more, and small is mighty. |
| first_indexed | 2024-09-23T12:08:43Z |
| format | Article |
| id | mit-1721.1/128881 |
| institution | Massachusetts Institute of Technology |
| language | English |
| last_indexed | 2024-09-23T12:08:43Z |
| publishDate | 2020 |
| publisher | Springer Science and Business Media LLC |
| record_format | dspace |
| spelling | mit-1721.1/1288812022-09-28T00:28:13Z Small and mighty: adaptation of superphylum Patescibacteria to groundwater environment drives their genome simplicity Tian, Renmao Ning, Daliang He, Zhili Zhang, Ping Spencer, Sarah J. Gao, Shuhong Shi, Weiling Wu, Linwei Zhang, Ya Yang, Yunfeng Adams, Benjamin G. Rocha, Andrea M. Detienne, Brittny L. Lowe, Kenneth A. Joyner, Dominique C. Klingeman, Dawn M. Arkin, Adam P. Fields, Matthew W. Hazen, Terry C. Stahl, David A. Alm, Eric J Zhou, Jizhong Massachusetts Institute of Technology. Department of Biological Engineering Massachusetts Institute of Technology. Department of Civil and Environmental Engineering Background: The newly defined superphylum Patescibacteria such as Parcubacteria (OD1) and Microgenomates (OP11) has been found to be prevalent in groundwater, sediment, lake, and other aquifer environments. Recently increasing attention has been paid to this diverse superphylum including > 20 candidate phyla (a large part of the candidate phylum radiation, CPR) because it refreshed our view of the tree of life. However, adaptive traits contributing to its prevalence are still not well known. Results: Here, we investigated the genomic features and metabolic pathways of Patescibacteria in groundwater through genome-resolved metagenomics analysis of > 600 Gbp sequence data. We observed that, while the members of Patescibacteria have reduced genomes (~ 1 Mbp) exclusively, functions essential to growth and reproduction such as genetic information processing were retained. Surprisingly, they have sharply reduced redundant and nonessential functions, including specific metabolic activities and stress response systems. The Patescibacteria have ultra-small cells and simplified membrane structures, including flagellar assembly, transporters, and two-component systems. Despite the lack of CRISPR viral defense, the bacteria may evade predation through deletion of common membrane phage receptors and other alternative strategies, which may explain the low representation of prophage proteins in their genomes and lack of CRISPR. By establishing the linkages between bacterial features and the groundwater environmental conditions, our results provide important insights into the functions and evolution of this CPR group. Conclusions: We found that Patescibacteria has streamlined many functions while acquiring advantages such as avoiding phage invasion, to adapt to the groundwater environment. The unique features of small genome size, ultra-small cell size, and lacking CRISPR of this large lineage are bringing new understandings on life of Bacteria. Our results provide important insights into the mechanisms for adaptation of the superphylum in the groundwater environments, and demonstrate a case where less is more, and small is mighty. U.S. Department of Energy, Office of Biological and Environmental Research (Award DE-AC02-05CH11231) 2020-12-21T20:50:25Z 2020-12-21T20:50:25Z 2020-04 2020-01 2020-05-05T12:53:45Z Article http://purl.org/eprint/type/JournalArticle 2049-2618 https://hdl.handle.net/1721.1/128881 Tian, Renmao et al. "Small and mighty: adaptation of superphylum Patescibacteria to groundwater environment drives their genome simplicity." Microbiome 8, 1 (April 2020): 51 © 2020 The Author(s) en http://dx.doi.org/10.1186/s40168-020-00825-w Microbiome Creative Commons Attribution 4.0 International license https://creativecommons.org/licenses/by/4.0/ application/pdf Springer Science and Business Media LLC BioMed Central (BMC) |
| spellingShingle | Tian, Renmao Ning, Daliang He, Zhili Zhang, Ping Spencer, Sarah J. Gao, Shuhong Shi, Weiling Wu, Linwei Zhang, Ya Yang, Yunfeng Adams, Benjamin G. Rocha, Andrea M. Detienne, Brittny L. Lowe, Kenneth A. Joyner, Dominique C. Klingeman, Dawn M. Arkin, Adam P. Fields, Matthew W. Hazen, Terry C. Stahl, David A. Alm, Eric J Zhou, Jizhong Small and mighty: adaptation of superphylum Patescibacteria to groundwater environment drives their genome simplicity |
| title | Small and mighty: adaptation of superphylum Patescibacteria to groundwater environment drives their genome simplicity |
| title_full | Small and mighty: adaptation of superphylum Patescibacteria to groundwater environment drives their genome simplicity |
| title_fullStr | Small and mighty: adaptation of superphylum Patescibacteria to groundwater environment drives their genome simplicity |
| title_full_unstemmed | Small and mighty: adaptation of superphylum Patescibacteria to groundwater environment drives their genome simplicity |
| title_short | Small and mighty: adaptation of superphylum Patescibacteria to groundwater environment drives their genome simplicity |
| title_sort | small and mighty adaptation of superphylum patescibacteria to groundwater environment drives their genome simplicity |
| url | https://hdl.handle.net/1721.1/128881 |
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