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In-depth Spatiotemporal Characterization of Planktonic Archaeal and Bacterial Communities in North and South San Francisco Bay

  • Microbiology of Aquatic Systems
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Abstract

Despite being the largest estuary on the west coast of North America, no in-depth survey of microbial communities in San Francisco Bay (SFB) waters currently exists. In this study, we analyze bacterioplankton and archaeoplankton communities at several taxonomic levels and spatial extents (i.e., North versus South Bay) to reveal patterns in alpha and beta diversity. We assess communities using high-throughput sequencing of the 16S rRNA gene in 177 water column samples collected along a 150-km transect over a 2-year monthly time-series. In North Bay, the microbial community is strongly structured by spatial salinity changes while in South Bay seasonal variations dominate community dynamics. Along the steep salinity gradient in North Bay, we find that operational taxonomic units (OTUs; 97% identity) have higher site specificity than at coarser taxonomic levels and turnover (“species” replacement) is high, revealing a distinct brackish community (in oligo-, meso-, and polyhaline samples) from fresh and marine end-members. At coarser taxonomic levels (e.g., phylum, class), taxa are broadly distributed across salinity zones (i.e., present/abundant in a large number of samples) and brackish communities appear to be a mix of fresh and marine communities. We also observe variations in brackish communities between samples with similar salinities, likely related to differences in water residence times between North and South Bay. Throughout SFB, suspended particulate matter is positively correlated with richness and influences changes in beta diversity. Within several abundant groups, including the SAR11 clade (comprising up to 30% of reads in a sample), OTUs appear to be specialized to a specific salinity range. Some other organisms also showed pronounced seasonal abundance, including Synechococcus, Ca. Actinomarina, and Nitrosopumilus-like OTUs. Overall, this study represents the first in-depth spatiotemporal survey of SFB microbial communities and provides insight into how planktonic microorganisms have specialized to different niches along the salinity gradient.

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References

  1. Nichols FH, Cloern JE, Luoma SN, Peterson DH (1986) The modification of an estuary. Science 231:567–573. https://doi.org/10.1126/science.231.4738.567

    Article  CAS  PubMed  Google Scholar 

  2. Kimmerer W (2004) Open water processes of the San Francisco estuary: from physical forcing to biological responses. San Franc Estuary Watershed Sci:2

  3. Raimonet M, Cloern JE (2017) Estuary–ocean connectivity: fast physics, slow biology. Glob Change Biol 23:2345–2357. https://doi.org/10.1111/gcb.13546

    Article  Google Scholar 

  4. Cloern JE (2001) Our evolving conceptual model of the coastal eutrophication problem. Mar Ecol Prog Ser 210:223–253. https://doi.org/10.3354/meps210223

    Article  CAS  Google Scholar 

  5. Lucas LV, Koseff JR, Monismith SG, Thompson JK (2009) Shallow water processes govern system-wide phytoplankton bloom dynamics: a modeling study. J Mar Syst 75:70–86. https://doi.org/10.1016/j.jmarsys.2008.07.011

    Article  Google Scholar 

  6. Cloern JE, Jassby AD (2012) Drivers of change in estuarine-coastal ecosystems: discoveries from four decades of study in San Francisco Bay. Rev Geophys 50:RG4001. https://doi.org/10.1029/2012RG000397

    Article  Google Scholar 

  7. Schraga TS, Cloern JE (2017) Water quality measurements in San Francisco Bay by the U.S. Geological Survey, 1969–2015. Sci Data 4:170098. https://doi.org/10.1038/sdata.2017.98

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Beck MW, Jabusch TW, Trowbridge PR, Senn DB (2018) Four decades of water quality change in the upper San Francisco Estuary. Estuar Coast Shelf Sci 212:11–22. https://doi.org/10.1016/j.ecss.2018.06.021

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Cloern JE (2019) Patterns, pace, and processes of water-quality variability in a long-studied estuary. Limnol Oceanogr 64:S192–S208. https://doi.org/10.1002/lno.10958

    Article  CAS  Google Scholar 

  10. Cloern JE, Jassby AD, Schraga TS, Nejad E, Martin C (2017) Ecosystem variability along the estuarine salinity gradient: examples from long-term study of San Francisco Bay. Limnol Oceanogr 62:S272–S291. https://doi.org/10.1002/lno.10537

    Article  CAS  Google Scholar 

  11. Cloern JE (1987) Turbidity as a control on phytoplankton biomass and productivity in estuaries. Cont Shelf Res 7:1367–1381. https://doi.org/10.1016/0278-4343(87)90042-2

    Article  Google Scholar 

  12. Cloern JE, Dufford R (2005) Phytoplankton community ecology: principles applied in San Francisco Bay. Mar Ecol Prog Ser 285:11–28. https://doi.org/10.3354/meps285011

    Article  CAS  Google Scholar 

  13. Cloern JE, Jassby AD (2010) Patterns and scales of phytoplankton variability in estuarine–coastal ecosystems. Estuar Coasts 33:230–241. https://doi.org/10.1007/s12237-009-9195-3

    Article  CAS  Google Scholar 

  14. Sutula M, Kudela R, Hagy JD et al (2017) Novel analyses of long-term data provide a scientific basis for chlorophyll-a thresholds in San Francisco Bay. Estuar Coast Shelf Sci 197:107–118. https://doi.org/10.1016/j.ecss.2017.07.009

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Hollibaugh JT, Wong PS, Murrell MC (2000) Similarity of particle-associated and free-living bacterial communities in northern San Francisco Bay, California. Aquat Microb Ecol 21:103–114. https://doi.org/10.3354/ame021103

    Article  Google Scholar 

  16. Murray AE, Hollibaugh JT, Orrego C (1996) Phylogenetic compositions of bacterioplankton from two California estuaries compared by denaturing gradient gel electrophoresis of 16S rDNA fragments. Appl Environ Microbiol 62:2676–2680

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Stepanauskas R, Moran MA, Bergamaschi BA, Hollibaugh JT (2003) Covariance of bacterioplankton composition and environmental variables in a temperate delta system. Aquat Microb Ecol 31:14

    Article  Google Scholar 

  18. Lozupone CA, Knight R (2007) Global patterns in bacterial diversity. Proc Natl Acad Sci 104:11436–11440. https://doi.org/10.1073/pnas.0611525104

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Thompson LR, Sanders JG, McDonald D et al (2017) A communal catalogue reveals Earth’s multiscale microbial diversity. Nature 551:457–463. https://doi.org/10.1038/nature24621

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Paver SF, Muratore D, Newton RJ, Coleman ML (2018) Reevaluating the salty divide: phylogenetic specificity of transitions between marine and freshwater systems. mSystems 3:e00232-18. https://doi.org/10.1128/mSystems.00232-18

    Article  PubMed  PubMed Central  Google Scholar 

  21. Crump BC, Armbrust EV, Baross JA (1999) Phylogenetic analysis of particle-attached and free-living bacterial communities in the Columbia River, its estuary, and the adjacent coastal ocean. Appl Environ Microbiol 65:3192–3204

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Crump BC, Hopkinson CS, Sogin ML, Hobbie JE (2004) Microbial biogeography along an estuarine salinity gradient: combined influences of bacterial growth and residence time. Appl Environ Microbiol 70:1494–1505. https://doi.org/10.1128/AEM.70.3.1494-1505.2004

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Doherty M, Yager PL, Moran MA, Coles VJ, Fortunato CS, Krusche AV, Medeiros PM, Payet JP, Richey JE, Satinsky BM, Sawakuchi HO, Ward ND, Crump BC (2017) Bacterial biogeography across the Amazon River-Ocean Continuum. Front Microbiol 8. https://doi.org/10.3389/fmicb.2017.00882

  24. Fortunato CS, Crump BC (2011) Bacterioplankton community variation across river to ocean environmental gradients. Microb Ecol 62:374–382. https://doi.org/10.1007/s00248-011-9805-z

    Article  PubMed  Google Scholar 

  25. Fortunato CS, Herfort L, Zuber P, Baptista AM, Crump BC (2012) Spatial variability overwhelms seasonal patterns in bacterioplankton communities across a river to ocean gradient. ISME J 6:554–563. https://doi.org/10.1038/ismej.2011.135

    Article  CAS  PubMed  Google Scholar 

  26. Herlemann DP, Labrenz M, Jürgens K et al (2011) Transitions in bacterial communities along the 2000 km salinity gradient of the Baltic Sea. ISME J 5:1571–1579. https://doi.org/10.1038/ismej.2011.41

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Mason OU, Canter EJ, Gillies LE, Paisie TK, Roberts BJ (2016) Mississippi river plume enriches microbial diversity in the Northern Gulf of Mexico. Front Microbiol 7. https://doi.org/10.3389/fmicb.2016.01048

  28. Liu J, Yu S, Zhao M, He B, Zhang XH (2014) Shifts in archaeaplankton community structure along ecological gradients of Pearl Estuary. FEMS Microbiol Ecol 90:424–435. https://doi.org/10.1111/1574-6941.12404

    Article  CAS  PubMed  Google Scholar 

  29. Murrell MC, Hollibaugh JT, Silver MW, Wong PS (1999) Bacterioplankton dynamics in northern San Francisco Bay: Role of particle association and seasonal freshwater flow. Limnol Oceanogr 44:295–308. https://doi.org/10.4319/lo.1999.44.2.0295

    Article  Google Scholar 

  30. Satinsky BM, Crump BC, Smith CB, Sharma S, Zielinski BL, Doherty M, Meng J, Sun S, Medeiros PM, Paul JH, Coles VJ, Yager PL, Moran MA (2014) Microspatial gene expression patterns in the Amazon River Plume. Proc Natl Acad Sci 111:11085–11090. https://doi.org/10.1073/pnas.1402782111

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Apprill A, McNally S, Parsons R, Weber L (2015) Minor revision to V4 region SSU rRNA 806R gene primer greatly increases detection of SAR11 bacterioplankton. Aquat Microb Ecol 75:129–137. https://doi.org/10.3354/ame01753

    Article  Google Scholar 

  32. Parada AE, Needham DM, Fuhrman JA (2016) Every base matters: assessing small subunit rRNA primers for marine microbiomes with mock communities, time series and global field samples. Environ Microbiol 18:1403–1414. https://doi.org/10.1111/1462-2920.13023

    Article  CAS  PubMed  Google Scholar 

  33. Walters RA, Cheng RT, Conomos TJ (1985) Time scales of circulation and mixing processes of San Francisco Bay waters. Hydrobiologia 129:24–36. https://doi.org/10.1007/BF00048685

    Article  Google Scholar 

  34. Walters W, Hyde ER, Berg-Lyons D et al (2016) Improved bacterial 16S rRNA gene (V4 and V4-5) and fungal internal transcribed spacer marker gene primers for microbial community surveys. mSystems 1:e00009-15. https://doi.org/10.1128/mSystems.00009-15

    Article  PubMed  Google Scholar 

  35. Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26:2460–2461. https://doi.org/10.1093/bioinformatics/btq461

    Article  CAS  PubMed  Google Scholar 

  36. Katoh K, Misawa K, Kuma K, Miyata T (2002) MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res 30:3059–3066

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Peña AG, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Turnbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336. https://doi.org/10.1038/nmeth.f.303

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Callahan BJ, Sankaran K, Fukuyama JA et al (2016) Bioconductor workflow for microbiome data analysis: from raw reads to community analyses. F1000Research 5:1492. https://doi.org/10.12688/f1000research.8986.1

    Article  PubMed  PubMed Central  Google Scholar 

  39. McMurdie PJ, Holmes S (2014) Waste not, want not: why rarefying microbiome data is inadmissible. PLOS Comput Biol 10:4f. https://doi.org/10.1371/journal.pcbi.1003531

    Article  CAS  Google Scholar 

  40. Love MI, Huber W, Anders S (2014) Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol 15:550. https://doi.org/10.1186/s13059-014-0550-8

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. McMurdie PJ, Holmes S (2013) phyloseq: An R package for reproducible interactive analysis and graphics of microbiome census data. PLOS ONE 8:e61217. https://doi.org/10.1371/journal.pone.0061217

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Oksanen J, Blanchet FG, Friendly M, et al (2018) vegan: Community Ecology Package

  43. Battaglia B (1959) Final resolution of the symposium on the classification of brackish waters. Archo Oceanogr Limnol 11(suppl):243–248

    Google Scholar 

  44. Almeida-Neto M, Guimarães P, Guimarães PR et al (2008) A consistent metric for nestedness analysis in ecological systems: reconciling concept and measurement. Oikos 117:1227–1239. https://doi.org/10.1111/j.0030-1299.2008.16644.x

    Article  Google Scholar 

  45. Wear EK, Wilbanks EG, Nelson CE, Carlson CA (2018) Primer selection impacts specific population abundances but not community dynamics in a monthly time-series 16S rRNA gene amplicon analysis of coastal marine bacterioplankton. Environ Microbiol 20:2709–2726. https://doi.org/10.1111/1462-2920.14091

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Novick E, Senn D (2014) External nutrient loads to San Francisco Bay. San Francisco Estuary Institute, Richmond

    Google Scholar 

  47. Hewson I, Fuhrman JA (2004) Richness and diversity of bacterioplankton species along an estuarine gradient in Moreton Bay, Australia. Appl Env Microbiol 70:3425–3433. https://doi.org/10.1128/AEM.70.6.3425-3433.2004

    Article  CAS  Google Scholar 

  48. Aguirre M, Abad D, Albaina A, Cralle L, Goñi-Urriza MS, Estonba A, Zarraonaindia I (2017) Unraveling the environmental and anthropogenic drivers of bacterial community changes in the Estuary of Bilbao and its tributaries. PLOS ONE 12:e0178755. https://doi.org/10.1371/journal.pone.0178755

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Baselga A (2010) Partitioning the turnover and nestedness components of beta diversity. Glob Ecol Biogeogr 19:134–143. https://doi.org/10.1111/j.1466-8238.2009.00490.x

    Article  Google Scholar 

  50. Liu J, Fu B, Yang H, Zhao M, He B, Zhang XH (2015) Phylogenetic shifts of bacterioplankton community composition along the Pearl Estuary: the potential impact of hypoxia and nutrients. Front Microbiol 6. https://doi.org/10.3389/fmicb.2015.00064

  51. Mehrshad M, Amoozegar MA, Ghai R, Shahzadeh Fazeli SA, Rodriguez-Valera F (2016) Genome reconstruction from metagenomic data sets reveals novel microbes in the brackish waters of the Caspian Sea. Appl Environ Microbiol 82:1599–1612. https://doi.org/10.1128/AEM.03381-15

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Hugerth LW, Larsson J, Alneberg J, Lindh MV, Legrand C, Pinhassi J, Andersson AF (2015) Metagenome-assembled genomes uncover a global brackish microbiome. Genome Biol 16:279. https://doi.org/10.1186/s13059-015-0834-7

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Bouvier TC, del Giorgio PA (2002) Compositional changes in free-living bacterial communities along a salinity gradient in two temperate estuaries. Limnol Oceanogr 47:453–470. https://doi.org/10.4319/lo.2002.47.2.0453

    Article  CAS  Google Scholar 

  54. Zhang Y, Jiao NZ, 焦念志, et al (2006) Contribution of major bacterial groups to bacterial biomass production along a salinity gradient in the South China Sea

  55. Kan J, Evans SE, Chen F, Suzuki MT (2008) Novel estuarine bacterioplankton in rRNA operon libraries from the Chesapeake Bay. Aquat Microb Ecol 51:55–66. https://doi.org/10.3354/ame01177

    Article  Google Scholar 

  56. Henson MW, Lanclos VC, Faircloth BC, Thrash JC (2018) Cultivation and genomics of the first freshwater SAR11 (LD12) isolate. ISME J 12:1846–1860. https://doi.org/10.1038/s41396-018-0092-2

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Vergin KL, Beszteri B, Monier A, Cameron Thrash J, Temperton B, Treusch AH, Kilpert F, Worden AZ, Giovannoni SJ (2013) High-resolution SAR11 ecotype dynamics at the Bermuda Atlantic Time-series Study site by phylogenetic placement of pyrosequences. ISME J 7:1322–1332. https://doi.org/10.1038/ismej.2013.32

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Shaw AK, Halpern AL, Beeson K, Tran B, Venter JC, Martiny JBH (2008) It’s all relative: ranking the diversity of aquatic bacterial communities. Environ Microbiol 10:2200–2210. https://doi.org/10.1111/j.1462-2920.2008.01626.x

    Article  PubMed  Google Scholar 

  59. Campbell BJ, Kirchman DL (2013) Bacterial diversity, community structure and potential growth rates along an estuarine salinity gradient. ISME J 7:210–220. https://doi.org/10.1038/ismej.2012.93

    Article  CAS  PubMed  Google Scholar 

  60. Herlemann DPR, Woelk J, Labrenz M, Jürgens K (2014) Diversity and abundance of “Pelagibacterales” (SAR11) in the Baltic Sea salinity gradient. Syst Appl Microbiol 37:601–604. https://doi.org/10.1016/j.syapm.2014.09.002

    Article  CAS  PubMed  Google Scholar 

  61. Smith MW, Herfort L, Fortunato CS, Crump BC, Simon HM (2017) Microbial players and processes involved in phytoplankton bloom utilization in the water column of a fast-flowing, river-dominated estuary. MicrobiologyOpen 6:e00467. https://doi.org/10.1002/mbo3.467

    Article  CAS  PubMed Central  Google Scholar 

  62. Williams TJ, Wilkins D, Long E, Evans F, DeMaere MZ, Raftery MJ, Cavicchioli R (2013) The role of planktonic Flavobacteria in processing algal organic matter in coastal East Antarctica revealed using metagenomics and metaproteomics. Environ Microbiol 15:1302–1317. https://doi.org/10.1111/1462-2920.12017

    Article  CAS  PubMed  Google Scholar 

  63. Alonso C, Warnecke F, Amann R, Pernthaler J (2007) High local and global diversity of Flavobacteria in marine plankton. Environ Microbiol 9:1253–1266. https://doi.org/10.1111/j.1462-2920.2007.01244.x

    Article  CAS  PubMed  Google Scholar 

  64. Gómez-Pereira PR, Fuchs BM, Alonso C, Oliver MJ, van Beusekom JEE, Amann R (2010) Distinct flavobacterial communities in contrasting water masses of the North Atlantic Ocean. ISME J 4:472–487. https://doi.org/10.1038/ismej.2009.142

    Article  CAS  PubMed  Google Scholar 

  65. Yang C, Li Y, Zhou B, Zhou Y, Zheng W, Tian Y, van Nostrand JD, Wu L, He Z, Zhou J, Zheng T (2015) Illumina sequencing-based analysis of free-living bacterial community dynamics during an Akashiwo sanguine bloom in Xiamen sea, China. Sci Rep 5:8476. https://doi.org/10.1038/srep08476

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Bennke CM, Krüger K, Kappelmann L, Huang S, Gobet A, Schüler M, Barbe V, Fuchs BM, Michel G, Teeling H, Amann RI (2016) Polysaccharide utilisation loci of Bacteroidetes from two contrasting open ocean sites in the North Atlantic. Environ Microbiol 18:4456–4470. https://doi.org/10.1111/1462-2920.13429

    Article  CAS  PubMed  Google Scholar 

  67. Seo J-H, Kang I, Yang S-J, Cho J-C (2017) Characterization of spatial distribution of the bacterial community in the South Sea of Korea. PLoS ONE 12:e0174159. https://doi.org/10.1371/journal.pone.0174159

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Ngugi DK, Stingl U (2018) High-quality draft single-cell genome sequence of the NS5 Marine Group from the Coastal Red Sea. Genome Announc 6:e00565–e00518. https://doi.org/10.1128/genomeA.00565-18

    Article  PubMed  PubMed Central  Google Scholar 

  69. Glöckner FO, Zaichikov E, Belkova N et al (2000) Comparative 16S rRNA analysis of Lake Bacterioplankton reveals globally distributed phylogenetic clusters including an abundant group of Actinobacteria. Appl Environ Microbiol 66:5053–5065. https://doi.org/10.1128/AEM.66.11.5053-5065.2000

    Article  PubMed  PubMed Central  Google Scholar 

  70. Kirchman DL, Dittel AI, Malmstrom RR, Cottrell MT (2005) Biogeography of major bacterial groups in the Delaware Estuary. Limnol Oceanogr 50:1697–1706. https://doi.org/10.4319/lo.2005.50.5.1697

    Article  CAS  Google Scholar 

  71. Holmfeldt K, Dziallas C, Titelman J, Pohlmann K, Grossart HP, Riemann L (2009) Diversity and abundance of freshwater Actinobacteria along environmental gradients in the brackish northern Baltic Sea. Environ Microbiol 11:2042–2054. https://doi.org/10.1111/j.1462-2920.2009.01925.x

    Article  CAS  PubMed  Google Scholar 

  72. Ghai R, Mizuno CM, Picazo A, Camacho A, Rodriguez-Valera F (2014) Key roles for freshwater Actinobacteria revealed by deep metagenomic sequencing. Mol Ecol 23:6073–6090. https://doi.org/10.1111/mec.12985

    Article  CAS  PubMed  Google Scholar 

  73. Cloern JE (1996) Phytoplankton bloom dynamics in coastal ecosystems: a review with some general lessons from sustained investigation of San Francisco Bay, California. Rev Geophys 34:127–168. https://doi.org/10.1029/96RG00986

    Article  CAS  Google Scholar 

  74. Cloern JE (2018) Why large cells dominate estuarine phytoplankton. Limnol Oceanogr 63:S392–S409. https://doi.org/10.1002/lno.10749

    Article  Google Scholar 

  75. Li WKW (1998) Annual average abundance of heterotrophic bacteria and Synechococcus in surface ocean waters. Limnol Oceanogr 43:1746–1753. https://doi.org/10.4319/lo.1998.43.7.1746

    Article  Google Scholar 

  76. Wang K, Wommack KE, Chen F (2011) Abundance and distribution of Synechococcus spp. and Cyanophages in the Chesapeake Bay. Appl Environ Microbiol 77:7459–7468. https://doi.org/10.1128/AEM.00267-11

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. Ahlgren NA, Rocap G (2012) Diversity and distribution of marine Synechococcus: multiple gene phylogenies for consensus classification and development of qPCR assays for sensitive measurement of clades in the ocean. Aquat Microbiol 3:213. https://doi.org/10.3389/fmicb.2012.00213

    Article  CAS  Google Scholar 

  78. Xia X, Vidyarathna NK, Palenik B, Lee P, Liu H (2015) Comparison of the seasonal variations of Synechococcus assemblage structures in estuarine waters and coastal waters of Hong Kong. Appl Environ Microbiol 81:7644–7655. https://doi.org/10.1128/AEM.01895-15

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  79. Ghai R, Mizuno CM, Picazo A et al (2013) Metagenomics uncovers a new group of low GC and ultra-small marine Actinobacteria. Sci Rep 3:srep02471. https://doi.org/10.1038/srep02471

    Article  Google Scholar 

  80. Mizuno CM, Rodriguez-Valera F, Ghai R (2015) Genomes of planktonic Acidimicrobiales: widening horizons for marine Actinobacteria by metagenomics. mBio 6:e02083-14. https://doi.org/10.1128/mBio.02083-14

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  81. Xie W, Luo H, Murugapiran SK, Dodsworth JA, Chen S, Sun Y, Hedlund BP, Wang P, Fang H, Deng M, Zhang CL (2018) Localized high abundance of Marine Group II archaea in the subtropical Pearl River Estuary: implications for their niche adaptation. Environ Microbiol 20:734–754. https://doi.org/10.1111/1462-2920.14004

    Article  CAS  PubMed  Google Scholar 

  82. Orellana LH, Ben Francis T, Krüger K, Teeling H, Müller MC, Fuchs BM, Konstantinidis KT, Amann RI (2019) Niche differentiation among annually recurrent coastal Marine Group II Euryarchaeota. ISME J 13:1–13. https://doi.org/10.1038/s41396-019-0491-z

    Article  CAS  Google Scholar 

  83. Mosier AC, Lund MB, Francis CA (2012) Ecophysiology of an ammonia-oxidizing archaeon adapted to low-salinity habitats. Microb Ecol 64:955–963. https://doi.org/10.1007/s00248-012-0075-1

    Article  CAS  PubMed  Google Scholar 

  84. Blainey PC, Mosier AC, Potanina A, Francis CA, Quake SR (2011) Genome of a low-salinity ammonia-oxidizing archaeon determined by single-cell and metagenomic analysis. PLOS ONE 6:e16626. https://doi.org/10.1371/journal.pone.0016626

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  85. Santoro AE, Dupont CL, Richter RA, Craig MT, Carini P, McIlvin MR, Yang Y, Orsi WD, Moran DM, Saito MA (2015) Genomic and proteomic characterization of “Candidatus Nitrosopelagicus brevis”: An ammonia-oxidizing archaeon from the open ocean. Proc Natl Acad Sci 112:1173–1178. https://doi.org/10.1073/pnas.1416223112

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  86. Wankel SD, Kendall C, Francis CA, Paytan A (2006) Nitrogen sources and cycling in the San Francisco Bay Estuary: a nitrate dual isotopic composition approach. Limnol Oceanogr 51:1654–1664. https://doi.org/10.4319/lo.2006.51.4.1654

    Article  CAS  Google Scholar 

  87. Damashek J, Casciotti KL, Francis CA (2016) Variable nitrification rates across environmental gradients in turbid, nutrient-rich estuary waters of San Francisco Bay. Estuaries Coasts 39:1050–1071

    Article  CAS  Google Scholar 

  88. Simonato F, Gómez-Pereira PR, Fuchs BM, Amann R (2010) Bacterioplankton diversity and community composition in the Southern Lagoon of Venice. Syst Appl Microbiol 33:128–138. https://doi.org/10.1016/j.syapm.2009.12.006

    Article  CAS  PubMed  Google Scholar 

  89. Hollibaugh J, Gifford S, Moran MA et al (2014) Seasonal variation in the metratranscriptomes of a Thaumarchaeota population from SE USA coastal waters. ISME J 8:685–698. https://doi.org/10.1038/ismej.2013.171

    Article  CAS  PubMed  Google Scholar 

  90. Schaefer SC, Hollibaugh JT (2017) Temperature decouples ammonium and nitrite oxidation in coastal waters. Environ Sci Technol 51:3157–3164. https://doi.org/10.1021/acs.est.6b03483

    Article  CAS  PubMed  Google Scholar 

  91. Laperriere SM, Nidzieko NJ, Fox RJ, Fisher AW, Santoro AE (2018) Observations of variable ammonia oxidation and nitrous oxide flux in a eutrophic estuary. Estuar Coasts. 42:33–44. https://doi.org/10.1007/s12237-018-0441-4

    Article  CAS  Google Scholar 

  92. Hu A, Yang Z, Yu C-P, Jiao N (2013) Dynamics of autotrophic marine planktonic Thaumarchaeota in the East China Sea. PLoS ONE 8:e61087. https://doi.org/10.1371/journal.pone.0061087

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  93. Kim J-G, Gwak J-H, Jung M-Y, An SU, Hyun JH, Kang S, Rhee SK (2019) Distinct temporal dynamics of planktonic archaeal and bacterial assemblages in the bays of the Yellow Sea. PLOS ONE 14:e0221408. https://doi.org/10.1371/journal.pone.0221408

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  94. Pitcher A, Wuchter C, Siedenberg K, Schouten S, Sinninghe Damsté JS (2011) Crenarchaeol tracks winter blooms of ammonia-oxidizing Thaumarchaeota in the coastal North Sea. Limnol Oceanogr 56:2308–2318. https://doi.org/10.4319/lo.2011.56.6.2308

    Article  CAS  Google Scholar 

  95. Wuchter C, Abbas B, Coolen MJL, Herfort L, van Bleijswijk J, Timmers P, Strous M, Teira E, Herndl GJ, Middelburg JJ, Schouten S, Sinninghe Damste JS (2006) Archaeal nitrification in the ocean. Proc Natl Acad Sci U S A 103:12317–12322. https://doi.org/10.1073/pnas.0600756103

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  96. Hollibaugh JT, Wong PS (1999) Microbial processes in the San Francisco Bay estuarine turbidity maximum. Estuaries 22:848–862. https://doi.org/10.2307/1353066

    Article  CAS  Google Scholar 

  97. Crump BC, Baross JA, Simenstad CA (1998) Dominance of particle-attached bacteria in the Columbia River estuary, USA. Aquat Microb Ecol 14:7–18. https://doi.org/10.3354/ame014007

    Article  Google Scholar 

  98. Smith MW, Zeigler Allen L, Allen AE, Herfort L, Simon HM (2013) Contrasting genomic properties of free-living and particle-attached microbial assemblages within a coastal ecosystem. Aquat Microbiol 4:120. https://doi.org/10.3389/fmicb.2013.00120

    Article  CAS  Google Scholar 

  99. Wang Y, Pan J, Yang J, Zhou Z, Pan Y, Li M (2019) Patterns and processes of free-living and particle-associated bacterioplankton and archaeaplankton communities in a subtropical river-bay system in South China. Limnol Oceanogr 0: https://doi.org/10.1002/lno.11314

  100. Li J-L, Salam N, Wang P-D, Chen LX, Jiao JY, Li X, Xian WD, Han MX, Fang BZ, Mou XZ, Li WJ (2018) Discordance between resident and active bacterioplankton in free-living and particle-associated communities in estuary ecosystem. Microb Ecol 76:637–647. https://doi.org/10.1007/s00248-018-1174-4

    Article  PubMed  Google Scholar 

  101. Dupont CL, Larsson J, Yooseph S, Ininbergs K, Goll J, Asplund-Samuelsson J, McCrow JP, Celepli N, Allen LZ, Ekman M, Lucas AJ, Hagström Å, Thiagarajan M, Brindefalk B, Richter AR, Andersson AF, Tenney A, Lundin D, Tovchigrechko A, Nylander JAA, Brami D, Badger JH, Allen AE, Rusch DB, Hoffman J, Norrby E, Friedman R, Pinhassi J, Venter JC, Bergman B (2014) Functional tradeoffs underpin salinity-driven divergence in microbial community composition. PLOS ONE 9:e89549. https://doi.org/10.1371/journal.pone.0089549

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgments

Thank you to Jim Cloern and the Water Quality of San Francisco Bay monitoring group (including but not limited to Tara Schraga, Jessica Dyke, Amy Kleckner, Jennifer Teschler, Charlie Martin, and Jan Thompson) at USGS and the R/V Polaris crew for facilitating our participation in numerous cruises. This work was supported in part by NSF CAREER grant OCE-0847266 from the Biological Oceanography program (to CAF), the Stanford McGee research grant (JD), and NSF GRFP and Amherst College Fellowships (to ANR). The work conducted by the U.S. Department of Energy Joint Genome Institute, a DOE Office of Science User Facility, is supported by the Office of Science of the U.S. Department of Energy under Contract No. DE-AC02-05CH11231. Sequencing thanks to JGI CSP project 503022 to CAF. Special thanks to Tijana Glavino del Rio at JGI.

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Rasmussen, A.N., Damashek, J., Eloe-Fadrosh, E.A. et al. In-depth Spatiotemporal Characterization of Planktonic Archaeal and Bacterial Communities in North and South San Francisco Bay. Microb Ecol 81, 601–616 (2021). https://doi.org/10.1007/s00248-020-01621-7

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