The AEGEAN-169 clade of bacterioplankton is synonymous with SAR11 subclade V (HIMB59) and metabolically distinct
ABSTRACT Bacterioplankton of the SAR11 clade are the most abundant marine microorganisms and consist of numerous subclades spanning order-level divergence (Pelagibacterales). The assignment of the earliest diverging subclade V (a.k.a. HIMB59) to the Pelagibacterales is highly controversial, with mul...
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| Format: | Article |
| Language: | English |
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American Society for Microbiology
2023-06-01
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| Series: | mSystems |
| Subjects: | |
| Online Access: | https://journals.asm.org/doi/10.1128/msystems.00179-23 |
| _version_ | 1797792351820709888 |
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| author | Eric W. Getz V. Celeste Lanclos Conner Y. Kojima Chuankai Cheng Michael W. Henson Max Emil Schön Thijs J. G. Ettema Brant C. Faircloth J. Cameron Thrash |
| author_facet | Eric W. Getz V. Celeste Lanclos Conner Y. Kojima Chuankai Cheng Michael W. Henson Max Emil Schön Thijs J. G. Ettema Brant C. Faircloth J. Cameron Thrash |
| author_sort | Eric W. Getz |
| collection | DOAJ |
| description | ABSTRACT Bacterioplankton of the SAR11 clade are the most abundant marine microorganisms and consist of numerous subclades spanning order-level divergence (Pelagibacterales). The assignment of the earliest diverging subclade V (a.k.a. HIMB59) to the Pelagibacterales is highly controversial, with multiple recent phylogenetic studies placing them completely separate from SAR11. Other than through phylogenomics, subclade V has not received detailed examination due to limited genomes from this group. Here, we assessed the ecogenomic characteristics of subclade V to better understand the role of this group in comparison to the Pelagibacterales. We used a new isolate genome, recently released single-amplified genomes and metagenome-assembled genomes, and previously established SAR11 genomes to perform a comprehensive comparative genomics analysis. We paired this analysis with the recruitment of metagenomes spanning the open ocean, coastal, and brackish systems. Phylogenomics, average amino acid identity, and 16S rRNA gene phylogeny indicate that SAR11 subclade V is synonymous with the ubiquitous AEGEAN-169 clade and support the contention that this group represents a taxonomic family. AEGEAN-169 shared many bulk genome qualities with SAR11, such as streamlining and low GC content, but genomes were generally larger. AEGEAN-169 had overlapping distributions with SAR11 but was metabolically distinct from SAR11 in its potential to transport and utilize a broader range of sugars as well as in the transport of trace metals and thiamin. Thus, regardless of the ultimate phylogenetic placement of AEGEAN-169, these organisms have distinct metabolic capacities that likely allow them to differentiate their niche from canonical SAR11 taxa. IMPORTANCE One goal of marine microbiologists is to uncover the roles various microorganisms are playing in biogeochemical cycles. Success in this endeavor relies on differentiating groups of microbes and circumscribing their relationships. An early-diverging group (subclade V) of the most abundant bacterioplankton, SAR11, has recently been proposed as a separate lineage that does not share a most recent common ancestor. But beyond phylogenetics, little has been done to evaluate how these organisms compare with SAR11. Our work leverages dozens of new genomes to demonstrate the similarities and differences between subclade V and SAR11. In our analysis, we also establish that subclade V is synonymous with a group of bacteria established from 16S rRNA gene sequences, AEGEAN-169. Subclade V/AEGEAN-169 has clear metabolic distinctions from SAR11 and their shared traits point to remarkable convergent evolution if they do not share a most recent common ancestor. |
| first_indexed | 2024-03-13T02:31:56Z |
| format | Article |
| id | doaj.art-2187e11a17a1498db470b521e566a768 |
| institution | Directory Open Access Journal |
| issn | 2379-5077 |
| language | English |
| last_indexed | 2024-03-13T02:31:56Z |
| publishDate | 2023-06-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | mSystems |
| spelling | doaj.art-2187e11a17a1498db470b521e566a7682023-06-29T13:00:40ZengAmerican Society for MicrobiologymSystems2379-50772023-06-018310.1128/msystems.00179-23The AEGEAN-169 clade of bacterioplankton is synonymous with SAR11 subclade V (HIMB59) and metabolically distinctEric W. Getz0V. Celeste Lanclos1Conner Y. Kojima2Chuankai Cheng3Michael W. Henson4Max Emil Schön5Thijs J. G. Ettema6Brant C. Faircloth7J. Cameron Thrash8Department of Biological Sciences, University of Southern California , Los Angeles, California, USADepartment of Biological Sciences, University of Southern California , Los Angeles, California, USADepartment of Biological Sciences, University of Southern California , Los Angeles, California, USADepartment of Biological Sciences, University of Southern California , Los Angeles, California, USADepartment of Geophysical Sciences, University of Chicago , Chicago, Illinois, USADepartment of Cell and Molecular Biology, Science for Life Laboratory, Uppsala University , Uppsala, SwedenLaboratory of Microbiology, Wageningen University and Research , Wageningen, The NetherlandsDepartment of Biological Sciences and Museum of Natural Science, Louisiana State University , Baton Rouge, Louisiana, USADepartment of Biological Sciences, University of Southern California , Los Angeles, California, USAABSTRACT Bacterioplankton of the SAR11 clade are the most abundant marine microorganisms and consist of numerous subclades spanning order-level divergence (Pelagibacterales). The assignment of the earliest diverging subclade V (a.k.a. HIMB59) to the Pelagibacterales is highly controversial, with multiple recent phylogenetic studies placing them completely separate from SAR11. Other than through phylogenomics, subclade V has not received detailed examination due to limited genomes from this group. Here, we assessed the ecogenomic characteristics of subclade V to better understand the role of this group in comparison to the Pelagibacterales. We used a new isolate genome, recently released single-amplified genomes and metagenome-assembled genomes, and previously established SAR11 genomes to perform a comprehensive comparative genomics analysis. We paired this analysis with the recruitment of metagenomes spanning the open ocean, coastal, and brackish systems. Phylogenomics, average amino acid identity, and 16S rRNA gene phylogeny indicate that SAR11 subclade V is synonymous with the ubiquitous AEGEAN-169 clade and support the contention that this group represents a taxonomic family. AEGEAN-169 shared many bulk genome qualities with SAR11, such as streamlining and low GC content, but genomes were generally larger. AEGEAN-169 had overlapping distributions with SAR11 but was metabolically distinct from SAR11 in its potential to transport and utilize a broader range of sugars as well as in the transport of trace metals and thiamin. Thus, regardless of the ultimate phylogenetic placement of AEGEAN-169, these organisms have distinct metabolic capacities that likely allow them to differentiate their niche from canonical SAR11 taxa. IMPORTANCE One goal of marine microbiologists is to uncover the roles various microorganisms are playing in biogeochemical cycles. Success in this endeavor relies on differentiating groups of microbes and circumscribing their relationships. An early-diverging group (subclade V) of the most abundant bacterioplankton, SAR11, has recently been proposed as a separate lineage that does not share a most recent common ancestor. But beyond phylogenetics, little has been done to evaluate how these organisms compare with SAR11. Our work leverages dozens of new genomes to demonstrate the similarities and differences between subclade V and SAR11. In our analysis, we also establish that subclade V is synonymous with a group of bacteria established from 16S rRNA gene sequences, AEGEAN-169. Subclade V/AEGEAN-169 has clear metabolic distinctions from SAR11 and their shared traits point to remarkable convergent evolution if they do not share a most recent common ancestor.https://journals.asm.org/doi/10.1128/msystems.00179-23comparative genomicsSAR11AEGEAN-169HIMB59bacterioplankton |
| spellingShingle | Eric W. Getz V. Celeste Lanclos Conner Y. Kojima Chuankai Cheng Michael W. Henson Max Emil Schön Thijs J. G. Ettema Brant C. Faircloth J. Cameron Thrash The AEGEAN-169 clade of bacterioplankton is synonymous with SAR11 subclade V (HIMB59) and metabolically distinct mSystems comparative genomics SAR11 AEGEAN-169 HIMB59 bacterioplankton |
| title | The AEGEAN-169 clade of bacterioplankton is synonymous with SAR11 subclade V (HIMB59) and metabolically distinct |
| title_full | The AEGEAN-169 clade of bacterioplankton is synonymous with SAR11 subclade V (HIMB59) and metabolically distinct |
| title_fullStr | The AEGEAN-169 clade of bacterioplankton is synonymous with SAR11 subclade V (HIMB59) and metabolically distinct |
| title_full_unstemmed | The AEGEAN-169 clade of bacterioplankton is synonymous with SAR11 subclade V (HIMB59) and metabolically distinct |
| title_short | The AEGEAN-169 clade of bacterioplankton is synonymous with SAR11 subclade V (HIMB59) and metabolically distinct |
| title_sort | aegean 169 clade of bacterioplankton is synonymous with sar11 subclade v himb59 and metabolically distinct |
| topic | comparative genomics SAR11 AEGEAN-169 HIMB59 bacterioplankton |
| url | https://journals.asm.org/doi/10.1128/msystems.00179-23 |
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