Genome-Resolved Metagenomic Insights into Massive Seasonal Ammonia-Oxidizing Archaea Blooms in San Francisco Bay
ABSTRACT Ammonia-oxidizing archaea (AOA) are key for the transformation of ammonia to oxidized forms of nitrogen in aquatic environments around the globe, including nutrient-rich coastal and estuarine waters such as San Francisco Bay (SFB). Using metagenomics and 16S rRNA gene amplicon libraries, we...
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| Format: | Article |
| Language: | English |
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American Society for Microbiology
2022-02-01
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| Series: | mSystems |
| Subjects: | |
| Online Access: | https://journals.asm.org/doi/10.1128/msystems.01270-21 |
| _version_ | 1818872266342006784 |
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| author | Anna N. Rasmussen Christopher A. Francis |
| author_facet | Anna N. Rasmussen Christopher A. Francis |
| author_sort | Anna N. Rasmussen |
| collection | DOAJ |
| description | ABSTRACT Ammonia-oxidizing archaea (AOA) are key for the transformation of ammonia to oxidized forms of nitrogen in aquatic environments around the globe, including nutrient-rich coastal and estuarine waters such as San Francisco Bay (SFB). Using metagenomics and 16S rRNA gene amplicon libraries, we found that AOA are more abundant than ammonia-oxidizing bacteria (AOB) and nitrite-oxidizing bacteria (NOB), except in the freshwater stations in SFB. In South SFB, we observed recurrent AOA blooms of “Candidatus Nitrosomarinus catalina” SPOT01-like organisms, which account for over 20% of 16S rRNA gene amplicons in both surface and bottom waters and co-occur with weeks of high nitrite concentrations (>10 μM) in the oxic water column. We observed pronounced nitrite peaks occurring in the autumn for 7 of the last 9 years (2012 to 2020), suggesting that seasonal AOA blooms are common in South SFB. We recovered two high-quality AOA metagenome-assembled genomes (MAGs), including a Nitrosomarinus-like genome from the South SFB bloom and another Nitrosopumilus genome originating from Suisun Bay in North SFB. Both MAGs cluster with genomes from other estuarine/coastal sites. Analysis of Nitrosomarinus-like genomes show that they are streamlined, with low GC content and high coding density, and harbor urease genes. Our findings support the unique niche of Nitrosomarinus-like organisms which dominate coastal/estuarine waters and provide insights into recurring AOA blooms in SFB. IMPORTANCE Ammonia-oxidizing archaea (AOA) carry out key transformations of ammonia in estuarine systems such as San Francisco Bay (SFB)—the largest estuary on the west coast of North America—and play a significant role in both local and global nitrogen cycling. Using metagenomics and 16S rRNA gene amplicon libraries, we document a massive, recurrent AOA bloom in South SFB that co-occurs with months of high nitrite concentrations in the oxic water column. Our study is the first to generate metagenome-assembled genomes (MAGs) from SFB, and through this process we recovered two high-quality AOA MAGs, one of which originated from bloom samples. These AOA MAGs yield new insight into the Nitrosopumilus and Nitrosomarinus-like lineages and their potential niches in coastal and estuarine systems. Nitrosomarinus-like AOA are abundant in coastal regions around the globe, and we highlight the common occurrence of urease genes, low GC content, and range of salinity tolerances within this lineage. |
| first_indexed | 2024-12-19T12:36:05Z |
| format | Article |
| id | doaj.art-7acd6ec55c6b401d9382aaeb8e9651df |
| institution | Directory Open Access Journal |
| issn | 2379-5077 |
| language | English |
| last_indexed | 2024-12-19T12:36:05Z |
| publishDate | 2022-02-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | mSystems |
| spelling | doaj.art-7acd6ec55c6b401d9382aaeb8e9651df2022-12-21T20:21:08ZengAmerican Society for MicrobiologymSystems2379-50772022-02-017110.1128/msystems.01270-21Genome-Resolved Metagenomic Insights into Massive Seasonal Ammonia-Oxidizing Archaea Blooms in San Francisco BayAnna N. Rasmussen0Christopher A. Francis1Department of Earth System Science, Stanford University, Stanford, California, USADepartment of Earth System Science, Stanford University, Stanford, California, USAABSTRACT Ammonia-oxidizing archaea (AOA) are key for the transformation of ammonia to oxidized forms of nitrogen in aquatic environments around the globe, including nutrient-rich coastal and estuarine waters such as San Francisco Bay (SFB). Using metagenomics and 16S rRNA gene amplicon libraries, we found that AOA are more abundant than ammonia-oxidizing bacteria (AOB) and nitrite-oxidizing bacteria (NOB), except in the freshwater stations in SFB. In South SFB, we observed recurrent AOA blooms of “Candidatus Nitrosomarinus catalina” SPOT01-like organisms, which account for over 20% of 16S rRNA gene amplicons in both surface and bottom waters and co-occur with weeks of high nitrite concentrations (>10 μM) in the oxic water column. We observed pronounced nitrite peaks occurring in the autumn for 7 of the last 9 years (2012 to 2020), suggesting that seasonal AOA blooms are common in South SFB. We recovered two high-quality AOA metagenome-assembled genomes (MAGs), including a Nitrosomarinus-like genome from the South SFB bloom and another Nitrosopumilus genome originating from Suisun Bay in North SFB. Both MAGs cluster with genomes from other estuarine/coastal sites. Analysis of Nitrosomarinus-like genomes show that they are streamlined, with low GC content and high coding density, and harbor urease genes. Our findings support the unique niche of Nitrosomarinus-like organisms which dominate coastal/estuarine waters and provide insights into recurring AOA blooms in SFB. IMPORTANCE Ammonia-oxidizing archaea (AOA) carry out key transformations of ammonia in estuarine systems such as San Francisco Bay (SFB)—the largest estuary on the west coast of North America—and play a significant role in both local and global nitrogen cycling. Using metagenomics and 16S rRNA gene amplicon libraries, we document a massive, recurrent AOA bloom in South SFB that co-occurs with months of high nitrite concentrations in the oxic water column. Our study is the first to generate metagenome-assembled genomes (MAGs) from SFB, and through this process we recovered two high-quality AOA MAGs, one of which originated from bloom samples. These AOA MAGs yield new insight into the Nitrosopumilus and Nitrosomarinus-like lineages and their potential niches in coastal and estuarine systems. Nitrosomarinus-like AOA are abundant in coastal regions around the globe, and we highlight the common occurrence of urease genes, low GC content, and range of salinity tolerances within this lineage.https://journals.asm.org/doi/10.1128/msystems.01270-21estuaryammonia-oxidizing archaeaThaumarchaeotanitrificationbloompelagic |
| spellingShingle | Anna N. Rasmussen Christopher A. Francis Genome-Resolved Metagenomic Insights into Massive Seasonal Ammonia-Oxidizing Archaea Blooms in San Francisco Bay mSystems estuary ammonia-oxidizing archaea Thaumarchaeota nitrification bloom pelagic |
| title | Genome-Resolved Metagenomic Insights into Massive Seasonal Ammonia-Oxidizing Archaea Blooms in San Francisco Bay |
| title_full | Genome-Resolved Metagenomic Insights into Massive Seasonal Ammonia-Oxidizing Archaea Blooms in San Francisco Bay |
| title_fullStr | Genome-Resolved Metagenomic Insights into Massive Seasonal Ammonia-Oxidizing Archaea Blooms in San Francisco Bay |
| title_full_unstemmed | Genome-Resolved Metagenomic Insights into Massive Seasonal Ammonia-Oxidizing Archaea Blooms in San Francisco Bay |
| title_short | Genome-Resolved Metagenomic Insights into Massive Seasonal Ammonia-Oxidizing Archaea Blooms in San Francisco Bay |
| title_sort | genome resolved metagenomic insights into massive seasonal ammonia oxidizing archaea blooms in san francisco bay |
| topic | estuary ammonia-oxidizing archaea Thaumarchaeota nitrification bloom pelagic |
| url | https://journals.asm.org/doi/10.1128/msystems.01270-21 |
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