Genome-Resolved Metagenomic Insights into Massive Seasonal Ammonia-Oxidizing Archaea Blooms in San Francisco Bay

Rasmussen, Anna N.; Francis, Christopher A.

doi:10.1128/msystems.01270-21

Genome-Resolved Metagenomic Insights into Massive Seasonal Ammonia-Oxidizing Archaea Blooms in San Francisco Bay

Journal Article · Tue Jan 25 00:00:00 EST 2022 · mSystems

DOI:https://doi.org/10.1128/msystems.01270-21· OSTI ID:1983352

^[1]; ^[1]

Stanford Univ., CA (United States)

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.

View Accepted Manuscript (DOE)

Research Organization:: USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)

Sponsoring Organization:: National Science Foundation (NSF); USDOE Office of Science (SC)

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1983352

Journal Information:: mSystems, Journal Name: mSystems Journal Issue: 1 Vol. 7; ISSN 2379-5077

Publisher:: American Society for MicrobiologyCopyright Statement

Country of Publication:: United States

Language:: English

References (106)

Using Paired In Situ High Frequency Nitrate Measurements to Better Understand Controls on Nitrate Concentrations and Estimate Nitrification Rates in a Wastewater-Impacted River: PAIRED HIGH FREQUENCY NITRATE SENSORS Kraus, T. E. C.; O'Donnell, K.; Downing, B. D. Water Resources Research, Vol. 53, Issue 10 https://doi.org/10.1002/2017WR020670	journal	October 2017
Respirometric estimation of the oxygen affinity constants for biological ammonium and nitrite oxidation Guisasola, Albert; Jubany, Irene; Baeza, Juan A. Journal of Chemical Technology & Biotechnology, Vol. 80, Issue 4 https://doi.org/10.1002/jctb.1202	journal	January 2005
Biogeochemical and metagenomic analysis of nitrite accumulation in the Gulf of Mexico hypoxic zone Bristow, Laura A.; Sarode, Neha; Cartee, John Limnology and Oceanography, Vol. 60, Issue 5 https://doi.org/10.1002/lno.10130	journal	July 2015
Time scales of circulation and mixing processes of San Francisco Bay waters Walters, R. A.; Cheng, R. T.; Conomos, T. J. Hydrobiologia, Vol. 129, Issue 1 https://doi.org/10.1007/BF00048685	journal	October 1985
Benthic fluxes in San Francisco Bay Hammond, Douglas E.; Fuller, Christopher; Harmon, Dana Hydrobiologia, Vol. 129, Issue 1 https://doi.org/10.1007/BF00048688	journal	October 1985
Phytoplankton blooms and nitrogen productivity in San Francisco Bay Wilkerson, Frances P.; Dugdale, Richard C.; Hogue, Victoria E. Estuaries and Coasts, Vol. 29, Issue 3 https://doi.org/10.1007/BF02784989	journal	June 2006
Ecophysiology of an Ammonia-Oxidizing Archaeon Adapted to Low-Salinity Habitats Mosier, Annika C.; Lund, Marie B.; Francis, Christopher A. Microbial Ecology, Vol. 64, Issue 4 https://doi.org/10.1007/s00248-012-0075-1	journal	May 2012
In-depth Spatiotemporal Characterization of Planktonic Archaeal and Bacterial Communities in North and South San Francisco Bay Rasmussen, Anna N.; Damashek, Julian; Eloe-Fadrosh, Emiley A. Microbial Ecology, Vol. 81, Issue 3 https://doi.org/10.1007/s00248-020-01621-7	journal	November 2020
Nutrient Fluxes from Sediments in the San Francisco Bay Delta Cornwell, Jeffrey C.; Glibert, Patricia M.; Owens, Michael S. Estuaries and Coasts, Vol. 37, Issue 5 https://doi.org/10.1007/s12237-013-9755-4	journal	January 2014
Variable Nitrification Rates Across Environmental Gradients in Turbid, Nutrient-Rich Estuary Waters of San Francisco Bay Damashek, Julian; Casciotti, Karen L.; Francis, Christopher A. Estuaries and Coasts, Vol. 39, Issue 4 https://doi.org/10.1007/s12237-016-0071-7	journal	February 2016
Observations of Variable Ammonia Oxidation and Nitrous Oxide Flux in a Eutrophic Estuary Laperriere, Sarah M.; Nidzieko, Nicholas J.; Fox, Rebecca J. Estuaries and Coasts, Vol. 42, Issue 1 https://doi.org/10.1007/s12237-018-0441-4	journal	August 2018
Estuarine nitrite maxima and nitrifying bacteria (Ems-Dollard estuary) Helder, W.; De Vries, R. T. P. Netherlands Journal of Sea Research, Vol. 17, Issue 1 https://doi.org/10.1016/0077-7579(83)90002-9	journal	October 1983
Nitrogenous nutrient transformations in the spring and fall in the Chesapeake Bay Horrigan, S. G.; Montoya, J. P.; Nevins, J. L. Estuarine, Coastal and Shelf Science, Vol. 30, Issue 4 https://doi.org/10.1016/0272-7714(90)90004-B	journal	April 1990
The role of ammonium and nitrate in spring bloom development in San Francisco Bay Dugdale, Richard C.; Wilkerson, Frances P.; Hogue, Victoria E. Estuarine, Coastal and Shelf Science, Vol. 73, Issue 1-2, p. 17-29 https://doi.org/10.1016/j.ecss.2006.12.008	journal	June 2007
River flow and ammonium discharge determine spring phytoplankton blooms in an urbanized estuary Dugdale, Richard; Wilkerson, Frances; Parker, Alexander E. Estuarine, Coastal and Shelf Science, Vol. 115 https://doi.org/10.1016/j.ecss.2012.08.025	journal	December 2012
Salinity impact on ammonia oxidizers activity and amoA expression in estuarine sediments Santos, J. P.; Mendes, D.; Monteiro, M. Estuarine, Coastal and Shelf Science, Vol. 211 https://doi.org/10.1016/j.ecss.2017.09.001	journal	October 2018
Major – but rare – spring blooms in 2014 in San Francisco Bay Delta, California, a result of the long-term drought, increased residence time, and altered nutrient loads and forms Glibert, Patricia M.; Dugdale, Richard C.; Wilkerson, Frances Journal of Experimental Marine Biology and Ecology, Vol. 460 https://doi.org/10.1016/j.jembe.2014.06.001	journal	November 2014
BlastKOALA and GhostKOALA: KEGG Tools for Functional Characterization of Genome and Metagenome Sequences Kanehisa, Minoru; Sato, Yoko; Morishima, Kanae Journal of Molecular Biology, Vol. 428, Issue 4 https://doi.org/10.1016/j.jmb.2015.11.006	journal	February 2016
Elevated ammonium concentrations from wastewater discharge depress primary productivity in the Sacramento River and the Northern San Francisco Estuary Parker, Alexander E.; Dugdale, Richard C.; Wilkerson, Frances P. Marine Pollution Bulletin, Vol. 64, Issue 3 https://doi.org/10.1016/j.marpolbul.2011.12.016	journal	March 2012
A New Perspective on Microbes Formerly Known as Nitrite-Oxidizing Bacteria Daims, Holger; Lücker, Sebastian; Wagner, Michael Trends in Microbiology, Vol. 24, Issue 9 https://doi.org/10.1016/j.tim.2016.05.004	journal	September 2016
Light Irradiation Enables Rapid Start-Up of Nitritation through Suppressing nxrB Gene Expression and Stimulating Ammonia-Oxidizing Bacteria Wang, Lingfeng; Qiu, Shuang; Guo, Jianhua Environmental Science & Technology https://doi.org/10.1021/acs.est.1c04174	journal	September 2021
Temperature Decouples Ammonium and Nitrite Oxidation in Coastal Waters Schaefer, Sylvia C.; Hollibaugh, James T. Environmental Science & Technology, Vol. 51, Issue 6 https://doi.org/10.1021/acs.est.6b03483	journal	March 2017
Origin, causes and effects of increased nitrite concentrations in aquatic environments Philips, Sarah; Laanbroek, Hendrikus J.; Verstraete, Willy Reviews in Environmental Science and Bio/Technology, Vol. 1, Issue 2 https://doi.org/10.1023/A:1020892826575	journal	June 2002
Ammonia oxidation and ammonia-oxidizing bacteria and archaea from estuaries with differing histories of hypoxia Caffrey, Jane M.; Bano, Nasreen; Kalanetra, Karen The ISME Journal, Vol. 1, Issue 7 https://doi.org/10.1038/ismej.2007.79	journal	October 2007
Metatranscriptomic analysis of ammonia-oxidizing organisms in an estuarine bacterioplankton assemblage Hollibaugh, James T.; Gifford, Scott; Sharma, Shalabh The ISME Journal, Vol. 5, Issue 5 https://doi.org/10.1038/ismej.2010.172	journal	November 2010
Diversity, abundance and expression of nitrite reductase (nirK)-like genes in marine thaumarchaea Lund, Marie B.; Smith, Jason M.; Francis, Christopher A. The ISME Journal, Vol. 6, Issue 10 https://doi.org/10.1038/ismej.2012.40	journal	May 2012
Seasonal variation in the metratranscriptomes of a Thaumarchaeota population from SE USA coastal waters Hollibaugh, James T.; Gifford, Scott M.; Moran, Mary Ann The ISME Journal, Vol. 8, Issue 3 https://doi.org/10.1038/ismej.2013.171	journal	October 2013
dRep: a tool for fast and accurate genomic comparisons that enables improved genome recovery from metagenomes through de-replication Olm, Matthew R.; Brown, Christopher T.; Brooks, Brandon The ISME Journal, Vol. 11, Issue 12 https://doi.org/10.1038/ismej.2017.126	journal	July 2017
Fast gapped-read alignment with Bowtie 2 Langmead, Ben; Salzberg, Steven L. Nature Methods, Vol. 9, Issue 4 https://doi.org/10.1038/nmeth.1923	journal	March 2012
Binning metagenomic contigs by coverage and composition Alneberg, Johannes; Bjarnason, Brynjar Smári; de Bruijn, Ino Nature Methods, Vol. 11, Issue 11 https://doi.org/10.1038/nmeth.3103	journal	September 2014
DADA2: High-resolution sample inference from Illumina amplicon data Callahan, Benjamin J.; McMurdie, Paul J.; Rosen, Michael J. Nature Methods, Vol. 13, Issue 7 https://doi.org/10.1038/nmeth.3869	journal	May 2016
Differential co-occurrence relationships shaping ecotype diversification within Thaumarchaeota populations in the coastal ocean water column Reji, Linta; Tolar, Bradley B.; Smith, Jason M. The ISME Journal, Vol. 13, Issue 5 https://doi.org/10.1038/s41396-018-0311-x	journal	January 2019
Phylogenomics suggests oxygen availability as a driving force in Thaumarchaeota evolution Ren, Minglei; Feng, Xiaoyuan; Huang, Yongjie The ISME Journal, Vol. 13, Issue 9 https://doi.org/10.1038/s41396-019-0418-8	journal	April 2019
Niche differentiation among annually recurrent coastal Marine Group II Euryarchaeota Orellana, Luis H.; Ben Francis, T.; Krüger, Karen The ISME Journal, Vol. 13, Issue 12 https://doi.org/10.1038/s41396-019-0491-z	journal	August 2019
Expansion of Thaumarchaeota habitat range is correlated with horizontal transfer of ATPase operons Wang, Baozhan; Qin, Wei; Ren, Yi The ISME Journal, Vol. 13, Issue 12 https://doi.org/10.1038/s41396-019-0493-x	journal	August 2019
Alternative strategies of nutrient acquisition and energy conservation map to the biogeography of marine ammonia-oxidizing archaea Qin, Wei; Zheng, Yue; Zhao, Feng The ISME Journal, Vol. 14, Issue 10 https://doi.org/10.1038/s41396-020-0710-7	journal	July 2020
Genomes of Thaumarchaeota from deep sea sediments reveal specific adaptations of three independently evolved lineages Kerou, Melina; Ponce-Toledo, Rafael I.; Zhao, Rui The ISME Journal, Vol. 15, Issue 9 https://doi.org/10.1038/s41396-021-00962-6	journal	April 2021
Cyanate and urea are substrates for nitrification by Thaumarchaeota in the marine environment Kitzinger, Katharina; Padilla, Cory C.; Marchant, Hannah K. Nature Microbiology, Vol. 4, Issue 2 https://doi.org/10.1038/s41564-018-0316-2	journal	December 2018
A complete domain-to-species taxonomy for Bacteria and Archaea Parks, Donovan H.; Chuvochina, Maria; Chaumeil, Pierre-Alain Nature Biotechnology https://doi.org/10.1038/s41587-020-0501-8	journal	April 2020
Water quality measurements in San Francisco Bay by the U.S. Geological Survey, 1969–2015 Schraga, Tara S.; Cloern, James E. Scientific Data, Vol. 4, Issue 1 https://doi.org/10.1038/sdata.2017.98	journal	August 2017
RASTtk: A modular and extensible implementation of the RAST algorithm for building custom annotation pipelines and annotating batches of genomes Brettin, Thomas; Davis, James J.; Disz, Terry Scientific Reports, Vol. 5, Issue 1 https://doi.org/10.1038/srep08365	journal	February 2015
Genomics and taxonomy in diagnostics for food security: soft-rotting enterobacterial plant pathogens Pritchard, Leighton; Glover, Rachel H.; Humphris, Sonia Analytical Methods, Vol. 8, Issue 1 https://doi.org/10.1039/C5AY02550H	journal	January 2016
Genomic and proteomic characterization of “ Candidatus Nitrosopelagicus brevis”: An ammonia-oxidizing archaeon from the open ocean Santoro, Alyson E.; Dupont, Christopher L.; Richter, R. Alex Proceedings of the National Academy of Sciences, Vol. 112, Issue 4 https://doi.org/10.1073/pnas.1416223112	journal	January 2015
Hydrogen peroxide detoxification is a key mechanism for growth of ammonia-oxidizing archaea Kim, Jong-Geol; Park, Soo-Je; Sinninghe Damsté, Jaap S. Proceedings of the National Academy of Sciences, Vol. 113, Issue 28 https://doi.org/10.1073/pnas.1605501113	journal	June 2016
MEGAHIT: an ultra-fast single-node solution for large and complex metagenomics assembly via succinct de Bruijn graph Li, Dinghua; Liu, Chi-Man; Luo, Ruibang Bioinformatics, Vol. 31, Issue 10 https://doi.org/10.1093/bioinformatics/btv033	journal	January 2015
MaxBin 2.0: an automated binning algorithm to recover genomes from multiple metagenomic datasets Wu, Yu-Wei; Simmons, Blake A.; Singer, Steven W. Bioinformatics, Vol. 32, Issue 4 https://doi.org/10.1093/bioinformatics/btv638	journal	October 2015
GTDB-Tk: a toolkit to classify genomes with the Genome Taxonomy Database Chaumeil, Pierre-Alain; Mussig, Aaron J.; Hugenholtz, Philip Bioinformatics https://doi.org/10.1093/bioinformatics/btz848	journal	November 2019
The SEED and the Rapid Annotation of microbial genomes using Subsystems Technology (RAST) Overbeek, Ross; Olson, Robert; Pusch, Gordon D. Nucleic Acids Research, Vol. 42, Issue D1 https://doi.org/10.1093/nar/gkt1226	journal	November 2013
Cytoscape: A Software Environment for Integrated Models of Biomolecular Interaction Networks Shannon, P. Genome Research, Vol. 13, Issue 11 https://doi.org/10.1101/gr.1239303	journal	November 2003
CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes Parks, Donovan H.; Imelfort, Michael; Skennerton, Connor T. Genome Research, Vol. 25, Issue 7 https://doi.org/10.1101/gr.186072.114	journal	May 2015
metaSPAdes: a new versatile metagenomic assembler Nurk, Sergey; Meleshko, Dmitry; Korobeynikov, Anton Genome Research, Vol. 27, Issue 5 https://doi.org/10.1101/gr.213959.116	journal	March 2017
Every base matters: assessing small subunit rRNA primers for marine microbiomes with mock communities, time series and global field samples: Primers for marine microbiome studies Parada, Alma E.; Needham, David M.; Fuhrman, Jed A. Environmental Microbiology, Vol. 18, Issue 5 https://doi.org/10.1111/1462-2920.13023	journal	October 2015
Strangers in the archaeal world: osmostress-responsive biosynthesis of ectoine and hydroxyectoine by the marine thaumarchaeon Nitrosopumilus maritimus: Ectoine and hydroxyectoine biosynthesis in Archaea Widderich, Nils; Czech, Laura; Elling, Felix J. Environmental Microbiology, Vol. 18, Issue 4 https://doi.org/10.1111/1462-2920.13156	journal	January 2016
Genome and epigenome of a novel marine Thaumarchaeota strain suggest viral infection, phosphorothioation DNA modification and multiple restriction systems: Genome and epigenome of a new marine thaumarchaeon Ahlgren, Nathan A.; Chen, Yangyang; Needham, David M. Environmental Microbiology, Vol. 19, Issue 6 https://doi.org/10.1111/1462-2920.13768	journal	May 2017
Localized high abundance of Marine Group II archaea in the subtropical Pearl River Estuary: implications for their niche adaptation: High abundance of MGII in an estuary Xie, Wei; Luo, Haiwei; Murugapiran, Senthil K. Environmental Microbiology, Vol. 20, Issue 2 https://doi.org/10.1111/1462-2920.14004	journal	December 2017
Extensive nitrification and active ammonia oxidizers in two contrasting coastal systems of the Baltic Sea Happel, Elisabeth; Bartl, Ines; Voss, Maren Environmental Microbiology, Vol. 20, Issue 8 https://doi.org/10.1111/1462-2920.14293	journal	August 2018
Genomic adaptation to eutrophication of ammonia‐oxidizing archaea in the Pearl River estuary Zou, Dayu; Li, Yingdong; Kao, Shuh‐Ji Environmental Microbiology, Vol. 21, Issue 7 https://doi.org/10.1111/1462-2920.14613	journal	April 2019
Quantitative distribution of presumptive archaeal and bacterial nitrifiers in Monterey Bay and the North Pacific Subtropical Gyre Mincer, Tracy J.; Church, Matthew J.; Taylor, Lance Trent Environmental Microbiology, Vol. 9, Issue 5 https://doi.org/10.1111/j.1462-2920.2007.01239.x	journal	May 2007
Relative abundance and diversity of ammonia-oxidizing archaea and bacteria in the San Francisco Bay estuary Mosier, Annika C.; Francis, Christopher A. Environmental Microbiology, Vol. 10, Issue 11 https://doi.org/10.1111/j.1462-2920.2008.01764.x	journal	November 2008
Population ecology of nitrifying Archaea and Bacteria in the Southern California Bight Beman, J. Michael; Sachdeva, Rohan; Fuhrman, Jed A. Environmental Microbiology, Vol. 12, Issue 5 https://doi.org/10.1111/j.1462-2920.2010.02172.x	journal	February 2010
Differential photoinhibition of bacterial and archaeal ammonia oxidation Merbt, Stephanie N.; Stahl, David A.; Casamayor, Emilio O. FEMS Microbiology Letters, Vol. 327, Issue 1 https://doi.org/10.1111/j.1574-6968.2011.02457.x	journal	December 2011
Human Domination of Earth's Ecosystems Vitousek, P. M. Science, Vol. 277, Issue 5325 https://doi.org/10.1126/science.277.5325.494	journal	July 1997
Genomic Characteristics of a Novel Species of Ammonia-Oxidizing Archaea from the Jiulong River Estuary Zou, Dayu; Wan, Ru; Han, Lili Applied and Environmental Microbiology, Vol. 86, Issue 18 https://doi.org/10.1128/AEM.00736-20	journal	September 2020
amoA Gene Abundances and Nitrification Potential Rates Suggest that Benthic Ammonia-Oxidizing Bacteria and Not Archaea Dominate N Cycling in the Colne Estuary, United Kingdom Li, Jialin; Nedwell, David B.; Beddow, Jessica Applied and Environmental Microbiology, Vol. 81, Issue 1 https://doi.org/10.1128/AEM.02654-14	journal	January 2015
Genome Sequence of “ Candidatus Nitrosoarchaeum limnia” BG20, a Low-Salinity Ammonia-Oxidizing Archaeon from the San Francisco Bay Estuary Mosier, Annika C.; Allen, Eric E.; Kim, Maria Journal of Bacteriology, Vol. 194, Issue 8 https://doi.org/10.1128/JB.00007-12	journal	April 2012
Genome Sequence of “ Candidatus Nitrosopumilus salaria” BD31, an Ammonia-Oxidizing Archaeon from the San Francisco Bay Estuary Mosier, Annika C.; Allen, Eric E.; Kim, Maria Journal of Bacteriology, Vol. 194, Issue 8 https://doi.org/10.1128/JB.00013-12	journal	April 2012
Coastal Ocean Metagenomes and Curated Metagenome-Assembled Genomes from Marsh Landing, Sapelo Island (Georgia, USA) Damashek, Julian; Edwardson, Christian F.; Tolar, Bradley B. Microbiology Resource Announcements, Vol. 8, Issue 40 https://doi.org/10.1128/MRA.00934-19	journal	October 2019
Metagenome Sequencing of Prokaryotic Microbiota Collected from Rivers in the Upper Amazon Basin Santos-Júnior, Célio Dias; Kishi, Luciano Takeshi; Toyama, Danyelle Genome Announcements, Vol. 5, Issue 2 https://doi.org/10.1128/genomeA.01450-16	journal	January 2017
A Genus Definition for Bacteria and Archaea Based on a Standard Genome Relatedness Index Barco, R. A.; Garrity, G. M.; Scott, J. J. mBio, Vol. 11, Issue 1 https://doi.org/10.1128/mBio.02475-19	journal	January 2020
A Salicylate–Hypochlorite Method for Determining Ammonia in Seawater Bower, Carol E.; Holm-Hansen, Thomas Canadian Journal of Fisheries and Aquatic Sciences, Vol. 37, Issue 5 https://doi.org/10.1139/f80-106	journal	May 1980
Prodigal: prokaryotic gene recognition and translation initiation site identification Hyatt, Doug; Chen, Gwo-Liang; LoCascio, Philip F. BMC Bioinformatics, Vol. 11, Issue 1 https://doi.org/10.1186/1471-2105-11-119	journal	March 2010
The RAST Server: Rapid Annotations using Subsystems Technology Aziz, Ramy K.; Bartels, Daniela; Best, Aaron A. BMC Genomics, Vol. 9, Issue 1, Article No. 75 https://doi.org/10.1186/1471-2164-9-75	journal	January 2008
Genome-resolved metagenomics analysis provides insights into the ecological role of Thaumarchaeota in the Amazon River and its plume Pinto, Otávio H. B.; Silva, Thais F.; Vizzotto, Carla S. BMC Microbiology, Vol. 20, Issue 1 https://doi.org/10.1186/s12866-020-1698-x	journal	January 2020
Metagenome-assembled genomes uncover a global brackish microbiome Hugerth, Luisa W.; Larsson, John; Alneberg, Johannes Genome Biology, Vol. 16, Issue 1 https://doi.org/10.1186/s13059-015-0834-7	journal	December 2015
MetaWRAP—a flexible pipeline for genome-resolved metagenomic data analysis Uritskiy, Gherman V.; DiRuggiero, Jocelyne; Taylor, James Microbiome, Vol. 6, Issue 1 https://doi.org/10.1186/s40168-018-0541-1	journal	September 2018
Sparse and Compositionally Robust Inference of Microbial Ecological Networks Kurtz, Zachary D.; Müller, Christian L.; Miraldi, Emily R. PLOS Computational Biology, Vol. 11, Issue 5 https://doi.org/10.1371/journal.pcbi.1004226	journal	May 2015
Genome of a Low-Salinity Ammonia-Oxidizing Archaeon Determined by Single-Cell and Metagenomic Analysis Blainey, Paul C.; Mosier, Annika C.; Potanina, Anastasia PLoS ONE, Vol. 6, Issue 2 https://doi.org/10.1371/journal.pone.0016626	journal	February 2011
Ammonium Uptake by Phytoplankton Regulates Nitrification in the Sunlit Ocean Smith, Jason M.; Chavez, Francisco P.; Francis, Christopher A. PLoS ONE, Vol. 9, Issue 9 https://doi.org/10.1371/journal.pone.0108173	journal	September 2014
Distinct temporal dynamics of planktonic archaeal and bacterial assemblages in the bays of the Yellow Sea Kim, Jong-Geol; Gwak, Joo-Han; Jung, Man-Young PLOS ONE, Vol. 14, Issue 8 https://doi.org/10.1371/journal.pone.0221408	journal	August 2019
Cutadapt removes adapter sequences from high-throughput sequencing reads Martin, Marcel EMBnet.journal, Vol. 17, Issue 1 https://doi.org/10.14806/ej.17.1.200	journal	May 2011
Response of Lower Sacramento River phytoplankton to high-ammonium wastewater effluent Strong, Aaron L.; Mills, Matthew M.; Huang, Ivy B. Elementa: Science of the Anthropocene, Vol. 9, Issue 1 https://doi.org/10.1525/elementa.2021.040	journal	February 2021
Open Water Processes of the San Francisco Estuary: From Physical Forcing to Biological Responses [Open Water Processes of the San Francisco Estuary: From Physical Forcing to Biological Responses] Kimmerer, Wim J. San Francisco Estuary and Watershed Science, Vol. 2, Issue 1 https://doi.org/10.15447/sfews.2004v2iss1art1	journal	February 2004
Sources of Nitrogen and Phosphorus to Northern San Francisco Bay Hager, Stephen W.; Schemel, Laurence E. Estuaries, Vol. 15, Issue 1 https://doi.org/10.2307/1352708	journal	March 1992
Using DECIPHER v2.0 to Analyze Big Biological Sequence Data in R Wright, Erik,S. The R Journal, Vol. 8, Issue 1 https://doi.org/10.32614/RJ-2016-025	journal	January 2016
Significance of biomass and light availability to phytoplankton productivity in San Francisco Bay Cole, Be; Cloern, Je Marine Ecology Progress Series, Vol. 17 https://doi.org/10.3354/meps017015	journal	January 1984
Effect of CO and light on ammonium and nitrite oxidation by chemolithotrophic bacteria Vanzella, A.; Guerrero, Ma; Jones, Rd Marine Ecology Progress Series, Vol. 57 https://doi.org/10.3354/meps057069	journal	January 1989
Photoinhibition of marine nitrifying bacteria. I. Wavelength-dependent response Guerrero, Ma; Jones, Rd Marine Ecology Progress Series, Vol. 141 https://doi.org/10.3354/meps141183	journal	January 1996
Our evolving conceptual model of the coastal eutrophication problem Cloern, Je Marine Ecology Progress Series, Vol. 210 https://doi.org/10.3354/meps210223	journal	January 2001
Phytoplankton communities from San Francisco Bay Delta respond differently to oxidized and reduced nitrogen substratesâ€”even under conditions that would otherwise suggest nitrogen sufficiency Glibert, Patricia M.; Wilkerson, Frances P.; Dugdale, Richard C. Frontiers in Marine Science, Vol. 1 https://doi.org/10.3389/fmars.2014.00017	journal	July 2014
Insights on the marine microbial nitrogen cycle from isotopic approaches to nitrification Casciotti, Karen L.; Buchwald, Carolyn Frontiers in Microbiology, Vol. 3 https://doi.org/10.3389/fmicb.2012.00356	journal	January 2012
Benthic ammonia oxidizers differ in community structure and biogeochemical potential across a riverine delta Damashek, Julian; Smith, Jason M.; Mosier, Annika C. Frontiers in Microbiology, Vol. 5 https://doi.org/10.3389/fmicb.2014.00743	journal	January 2015
Hurricane Disturbance Stimulated Nitrification and Altered Ammonia Oxidizer Community Structure in Lake Okeechobee and St. Lucie Estuary (Florida) Hampel, Justyna J.; McCarthy, Mark J.; Aalto, Sanni L. Frontiers in Microbiology, Vol. 11 https://doi.org/10.3389/fmicb.2020.01541	journal	July 2020
Light as a Novel Inhibitor of Nitrite-Oxidizing Bacteria (NOB) for the Mainstream Partial Nitrification of Wastewater Treatment Kim, Keugtae; Park, Yong-Gyun Processes, Vol. 9, Issue 2 https://doi.org/10.3390/pr9020346	journal	February 2021
Chesapeake Bay nutrient and plankton dynamics. 2. Sources and sinks of nitrite1 McCarthy, James J.; Kaplan, Warren; Nevins, John L. Limnology and Oceanography, Vol. 29, Issue 1 https://doi.org/10.4319/lo.1984.29.1.0084	journal	January 1984
Oceanic and estuarine ammonium oxidation: Effects of light Horrigan, S. G.; Springer, A. L. Limnology and Oceanography, Vol. 35, Issue 2 https://doi.org/10.4319/lo.1990.35.2.0479	journal	March 1990
Trophic interactions and direct physical effects control phytoplankton biomass and production in an estuary Alpine, Andrea E.; Cloern, James E. Limnology and Oceanography, Vol. 37, Issue 5 https://doi.org/10.4319/lo.1992.37.5.0946	journal	July 1992
Crenarchaeol tracks winter blooms of ammonia-oxidizing Thaumarchaeota in the coastal North Sea Pitcher, Angela; Wuchter, Cornelia; Siedenberg, Kathi Limnology and Oceanography, Vol. 56, Issue 6 https://doi.org/10.4319/lo.2011.56.6.2308	journal	November 2011
Ammonia availability shapes the seasonal distribution and activity of archaeal and bacterial ammonia oxidizers in the Puget Sound Estuary Urakawa, Hidetoshi; Martens-Habbena, Willm; Huguet, Carme Limnology and Oceanography, Vol. 59, Issue 4 https://doi.org/10.4319/lo.2014.59.4.1321	journal	July 2014
Measurements of nitrite production in and around the primary nitrite maximum in the central California Current Santoro, A. E.; Sakamoto, C. M.; Smith, J. M. Biogeosciences, Vol. 10, Issue 11 https://doi.org/10.5194/bg-10-7395-2013	journal	January 2013
Diversity and distribution of amoA -type nitrifying and nirS -type denitrifying microbial communities in the Yangtze River estuary Zhang, Y.; Xie, X.; Jiao, N. Biogeosciences, Vol. 11, Issue 8 https://doi.org/10.5194/bg-11-2131-2014	journal	January 2014
Phytoplankton primary production in the world's estuarine-coastal ecosystems Cloern, J. E.; Foster, S. Q.; Kleckner, A. E. Biogeosciences, Vol. 11, Issue 9 https://doi.org/10.5194/bg-11-2477-2014	journal	May 2014
Niche differentiation of ammonia and nitrite oxidizers along a salinity gradient from the Pearl River estuary to the South China Sea Hou, Lei; Xie, Xiabing; Wan, Xianhui Biogeosciences, Vol. 15, Issue 16 https://doi.org/10.5194/bg-15-5169-2018	journal	August 2018
Metagenome-assembled genomes uncover a global brackish microbiome Hugerth, Luisa; Larsson, John; Alneberg, Johannes Figshare https://doi.org/10.6084/m9.figshare.c.3622883	collection	January 2015
Genome-resolved metagenomics analysis provides insights into the ecological role of Thaumarchaeota in the Amazon River and its plume Pinto, OtÃ¡Vio; Silva, Thais; Vizzotto, Carla figshare https://doi.org/10.6084/m9.figshare.c.4819383	collection	January 2020
Anvi’o: an advanced analysis and visualization platform for ‘omics data Eren, A. Murat; Esen, Özcan C.; Quince, Christopher PeerJ, Vol. 3 https://doi.org/10.7717/peerj.1319	journal	January 2015
MetaBAT 2: an adaptive binning algorithm for robust and efficient genome reconstruction from metagenome assemblies Kang, Dongwan D.; Li, Feng; Kirton, Edward PeerJ, Vol. 7 https://doi.org/10.7717/peerj.7359	journal	January 2019

Similar Records

Dynamics and activity of an ammonia-oxidizing archaea bloom in South San Francisco Bay

Journal Article · Mon Jul 29 20:00:00 EDT 2024 · The ISME Journal · OSTI ID:2434054

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
Thaumarchaeota
ammonia-oxidizing archaea
bloom
estuary
metagenome-assembled genome
microbiology
nitrification
pelagic

Genome-Resolved Metagenomic Insights into Massive Seasonal Ammonia-Oxidizing Archaea Blooms in San Francisco Bay

Citation Formats

References (106)

Similar Records

Related Subjects