Scientific Publications

BIOS-SCOPE Publications

2022-2021 Funding period
Bachy C., F. Wittmers, J. Muschiol, M.Hamilton, B. Henrissat, A.Z. Worden (2022) The Land–Sea Connection: Insights Into the Plant Lineage from a Green Algal Perspective. Annual Review of Plant Biology; doi: 10.1146/annurev-arplant-071921-100530

Bachy, C., E. Hehenberger, Y.-C. Ling, D.M. Needham, J. Strauss, S. Wilken, A.Z. Worden (2022) Marine Protists: A Hitchhiker’s Guide to their Role in the Marine Microbiome. The Marine Microbiome; doi: 10.1007/978-3-030-90383-1_4

Baetge, N., L.M. Bolaños, A.D. Penna, P. Gaube, S. Liu, K. Opalk, J.R. Graff, S. J. Giovannoni, M.J. Behrenfeld, C.A. Carlson. (2022) Bacterioplankton response to physical stratification following deep convection. Elementa doi.org/10.1525/elementa.2021.00078

*Bayer, B., et al. (2022). “Carbon content, carbon fixation yield and dissolved organic carbon release from diverse marine nitrifiers.” bioRxiv; Limnology and Oceanography- in press

Blanco-Bercial, L., R. Parsons, L.M. Bolaños, R. Johnson, G. Giovannoni, R. Curry (2022) The protist community traces seasonality and mesoscale hydrographic features in the oligotrophic Sargasso Sea. Frontiers in Marine Sciences, 9:897140.

Bolaños LM, Tait K, Somerfield PJ, Parsons RJ, Giovannoni SJ, Smyth T, Temperton B. (2022). Influence of short and long term processes on SAR11 communities in open ocean and coastal systems. bioRxiv:2022.06.17.496560. DOI: 10.1101/2022.06.17.496560.

Buchholz HH, Bolaños LM, Bell AG, Michelsen ML, Allen MJ, Temperton B. (2022). Pelagibacter phage Skadi – An abundant polar specialist that exemplifies ecotypic niche specificity among the most abundant viruses on Earth. bioRxiv:2022.08.10.503363. DOI: 10.1101/2022.08.10.503363.

Buchholz HH, Bolaños LM, Bell AG, Michelsen ML, Allen MJ, Temperton B. (2022). A Novel and Ubiquitous Marine Methylophage Provides Insights into Viral-Host Coevolution and Possible Host-Range Expansion in Streamlined Marine Heterotrophic Bacteria. Appl. Env. Micro. 88:e0025522.

Comstock, J., et al. “Bacterioplankton communities reveal horizontal and vertical influence of an Island Mass Effect.” Environmental Microbiology 24(9): 4193-4208. https://doi.org/10.1111/1462-2920.16092

*Eckmann C., C. Bachy, F. Wittmers, J. Strauss, L. Blanco-Bercial, K.L. Vergin, R.J. Parsons, S.J. Giovannoni, C.A.Carlson, A.Z. Worden (2022) Seasonal transitions in green algae expose niche and strategy differentiation in the Atlantic Ocean. Submitted to ISME J.

Halewood, E., Opalk, K., Custals, L., Carey, M., Hansell, D.A. and Carlson, C.A. (2022) GO-SHIP Repeat Hydrography: Determination of dissolved organic carbon (DOC) and total dissolved nitrogen (TDN) in seawater using High Temperature Combustion Analysis. Ocean Best Practices http://dx.doi.org/10.25607/OBP-1745.

*Johnson, W. M., M. C. Kido Soule, K. Longnecker, M. P. Bhatia, S. J. Hallam, M. W. Lomas and E. B. Kujawinski (revision submitted, September 2022). Insights into the controls on metabolite distributions along a latitudinal transect of the western Atlantic Ocean. bioRxiv preprint doi: https://doi.org/10.1101/2021.03.09.434501 Limnology and Oceanography.

Kim, S., I. Kang , J.W. Lee, C.O. Jeon, S.J. Giovannoni , and J.C. Cho. 2021. Heme auxotrophy in abundant aquatic microbial lineages. Proc. Natl. Acad. Sci. U.S.A. DOI: 10.1073/pnas.2102750118

*Lee, C.P., L.P. Collart, K.H. Halsey and S.J. Giovannoni. Quantitative seawater arsenic speciation by proton-transfer-reaction mass spectrometry. In Review.

Liu, S., K. Longnecker, E.B. Kujawinski, K.Vergin, L.M. Bolaños, S.J. Giovannoni, R. Parsons, K. Opalk, E. Halewood, D.A. Hansell, R. Johnson, R. Curry and C.A. Carlson. 2022.  Linkages Among Dissolved Organic Matter Export, Dissolved Metabolites, and Associated Microbial Community Structure Response in the Northwestern Sargasso Sea on a Seasonal Scale. Frontiers in Microbiol. doi.org/10.3389/fmicb.2022.833252

Moore, E.R., A. J. Weaver, E.W. Davis, S. J. Giovannoni, and K. H. Halsey. 2021. Metabolism of key atmospheric volatile organic compounds by the marine heterotrophic bacterium Pelagibacter HTCC1062 (SAR11). Environ. Microbiol. DOI: 10.1111/1462-2920.15837

*Noell, S.E., E.W. Davis II, F.L. Hellweger, and S.J. Giovannoni. Differences in regulatory strategies in marine oligotrophs and copiotrophs reflect differences in motility. bioRxiv preprint doi: https://doi.org/10.1101/2022.07.21.501054. In Review

*Villiot, N., A.E. Maas, A. Poulton, L. Blanco-Bercial. Organic and inorganic nutrients modulate taxonomic diversity and trophic strategies of small eukaryotes in oligotrophic oceans. In Review.

*Warwick-Dugdale JL, Tian F, Michelsen ML, Cronin DR, Moore K, Farbos A, Chittick L, Bell A, Buchholz HH, Parsons RJ, Zayed AA, Allen MJ, Sullivan MB, Temperton B. (2022). Long-read powered viral metagenomics in the oligotrophic Sargasso Sea. bioRxiv:2022.09.19.508504. DOI: 10.1101/2022.09.19.508504.

Wittmers, F., D. M. Needham, E. Hehenberger, S. J. Giovannoni, A.Z. Worden. 2021. Genomes from Uncultivated Pelagiphages Reveal Multiple Phylogenetic Clades Exhibiting Extensive Auxiliary Metabolic Genes and Cross-Family Multigene Transfers. mSystems https://doi.org/10.1128/msystems.01522-21

2021-2020 Funding Period
Bachy, C. & Yung, C-M., D.M. Needham, C. Gazitua, S. Roux, A.J. Limardo, C.J. Choi, M.B. Sullivan, A.Z. Worden (2021). Viruses infecting a warm water picoeukaryote shed light on spatial co-occurrence dynamics of marine viruses and their hosts. The ISME Journal. doi.org/10.1038/s41396-021-00989-9.

Buchholz, H.H., Michelsen, M.L., Bolaños, L.M. et al. Efficient dilution-to-extinction isolation of novel virus–host model systems for fastidious heterotrophic bacteria. ISME J 15, 1585–1598 (2021). https://doi.org/10.1038/s41396-020-00872-z

Buchholz, H. H., L. M. Bolaños, A. G. Bell, M. L. Michelsen, M. J. Allen and B. Temperton (2021). Genomic evidence for inter-class host transition between abundant streamlined heterotrophs by a novel and ubiquitous marine Methylophage. bioRxiv: 2021.2008.2024.457595.10.1101/2021.08.24.457595

Buchholz HH, Michelsen M, Parsons RJ, Bates NR, Temperton B. 2021b. Draft genome sequences of pelagimyophage Mosig EXVC030M and pelagipodophage Lederberg EXVC029P, isolated from Devil’s Hole, Bermuda. Microbiol Resour Announc 10: e01325-20. https://doi.org/10.1128/MRA.01325-20.

Cox, D. A., Parsons, R. J., Van Mooy, B. A. S. and Valentine, D. L. (Submitted). “Methylphosphonate is utilized by macroalgal holobionts in low nutrient environments”. Geophysical Research Letters.

Doherty, S.C., A.E. Maas, D.K. Steinberg, B.N. Popp, H.G. Close (2021) Distinguishing fecal pellets as a component of the biological pump using compound-specific isotope analysis of amino acids. Limnology and Oceanography, 66, 2827-2841.

Giovannoni S, Chan F, Davis E, II, Deutsch C, Wolf S. 2021. Biochemical barriers on the path to ocean anoxia? mBio 12:e01332-21. https://doi.org/10.1128/mBio.01332-21.

Johnson, W. M., M. C. Kido Soule, K. Longnecker, M. P. Bhatia, S. J. Hallam, M. W. Lomas and E. B. Kujawinski (submitted March 2021, in revision as of August 2021). Insights into the controls on metabolite distributions along a latitudinal transect of the western Atlantic Ocean. Limnology and Oceanography. DOI: 10.1101/2021.03.09.434501

Lee, C.P. , L.P. Collart, K. H. Halsey and S. J. Giovannoni. Quantitative seawater arsenic speciation by proton-transfer-reaction mass spectrometry. In Review.

Liu, S., Baetge, N., Comstock, J., Opalk, K., Parsons, R., Halewood, E., English, C.J., Giovannoni, S., Bolaños, L.M., Nelson, C.E. and Vergin, K., 2020. Stable isotope probing identifies bacterioplankton lineages capable of utilizing dissolved organic matter across a range of bioavailability. Frontiers in Microbiology 11: 2364. https://doi.org/10.3389/fmicb.2020.580397

Mayerhofer, M.M., Eigemann, F., Lackner, C. et al. Dynamic carbon flux network of a diverse marine microbial community. ISME COMMUN. 1, 50 (2021). https://doi.org/10.1038/s43705-021-00055-7

Moore, E.R., A. J. Weaver, E.W. Davis, S. J. Giovannoni, and K. H. Halsey. Metabolism of key atmospheric volatile organic compounds by the marine heterotrophic bacterium Pelagibacter HTCC1062 (SAR11). Environ. Microbiol. In Review

Noell SE, Barrell GE, Suffridge C, Morré, J, Gable KP, Graff JR, VerWey BJ, Hellweger FL,Giovannoni SJ. 2021. SAR11 cells rely on enzyme multifunctionality to metabolize a range of polyamine compounds. mBio 12:e01091-21. https://doi.org/10.1128/mBio.01091-21.

Noell, S.E., E.W. Davis II, F.L. Hellweger, and S.J. Giovannoni. Differences in regulatory strategies in marine oligotrophs and copiotrophs reflect differences in motility. In Review

Widner, B., M. C. Kido Soule, F. Ferrer-González, M. A. Moran and E. B. Kujawinski (2021). Quantification of amine- and alcohol-containing metabolites in saline samples using pre-extraction benzoyl chloride derivatization and ultra-high performance liquid chromatography tandem mass spectrometry (UHPLC MS/MS). Analytical Chemistry 93: 4809-4817. DOI: 10.1021/acs.analchem.0c03769.

Zablocki O, Michelsen M, Burris M, Solonenko N, Warwick-Dugdale J, Ghosh R, Pett-Ridge J, Sullivan MB, Temperton B. 2021. VirION2: a short- and long-read sequencing and informatics workflow to study the genomic diversity of viruses in nature. PeerJ 9:e11088 https://doi.org/10.7717/peerj.11088

2020-2019 Funding Period
Blanco-Bercial, L. (2020). Metabarcoding analysis and seasonality of the zooplankton community at BATS. Frontiers in Marine Science 7: 173. https://doi.org/10.3389/fmars.2020.00173

Foreman, R.K., Bjorkman, K.M., Carlson, C.A., Opalk, K., and Karl, D.M. (2019) Improved ultraviolet photo-oxidation system yields estimates for deep-sea dissolved organic nitrogen and phosphorus. Limnol. Oceanogr.: Methods, 17(4): 277-291. https://doi.org/10.1002/lom3.10312

Giovannoni, S.J., Halsey, K.H., Saw, J., Muslin, O., Suffridge, C., Sun, J., Lee, C., Moore, E.R., Temperton, B., and Noell, S. (2019). A parasitic arsenic cycle that shuttles energy from phytoplankton to heterotrophic baterioplankton. mBio 10(2)https://doi.org/10.1128/MbIO.00246-19

Johnson, W.M., Longnecker, K., Kido Soule, M.C., Arnold, W.A., Bhatia, M.P., Hallam, S.J., Van Mooy, B.A.S., and Kujawinski, E.B. (2019) Metabolite composition of sinking particles reflects a changing microbial community and differential metabolite degradation. Limnology and Oceanography 65(1): 111-127https://doi.org/10.1002/lno.11255

Liu, S., Parsons, R., Opalk, K., Baetge, N., Giovannoni, S., Bolanos, L.M., Kujawinski, E.B., Longnecker, K., Lu, Y., Halewood, E., Carlson, C.A. (2020). Different carboxyl-rich alicyclic molecules proxy compounds select distinct bacterioplankton for oxidation of dissolved organic matter in the mesopelagic Sargasso Sea. Limnology and Oceanography 65(7): 1532-1553. https://doi.org/10.1002/lno.11405

Maas, A.E., Liu, S., Bolaños, L.M., Widner, B., Parsons, R., Kujawinski, E.B., Blanco-Bercial, L. and Carlson, C.A., 2020. Migratory Zooplankton Excreta and Its Influence on Prokaryotic Communities. Frontiers in Marine Science https://doi.org/10.3389/fmars.2020.573268

McDonald, N., Achterberg, E.P., Carlson, C.A., Gledhill, M., Liu, S. Matheson-Barker, J.R., Nelson, N.B., Parsons, R.J. (2019). The role of heterotrophic bacteria and Archaea in the transformation of lignin in the open ocean. Frontiers in Marine Science 6:743. https://doi.org/10.3389/fmars.2019.00743

Saw, J.H.W., Nunoura, T., Hirai, M., Takaki, Y., Parsons, R., Michelsen, M., Longnecker, K., Kujawinski, E.B., Stepanauskas, R., Landry, Z., Carlson, C.A., and Giovannoni, S.J. (2020) Pangenomics reveal diversification of enzyme families and nich specialization in globally abundant SAR202 bacteria. mBio 11(1). https://doi.org/10.1128/mBio.02975-19

Wear, E.K., Carlson, C.A., Church, M.J. (2020). Bacterioplankton metabolism of phytoplankton lysates across a cyclone-anticyclone eddy dipole impacts the cycling of semi-labile matter in the photic zone. Limnology and Oceanography 65(7): 1608-1622. https://doi.org/10.1002/lno.11409

2019-2018 Funding Period
Foreman, R., K.M. Bjökman, C.A. Carlson, K. Opalk, and D.M. Karl (2018). Improved UV photo-oxidation system yields estimates for deep sea dissolved organic nitrogen and phosphorus. L&O Methods in press.

Landry, Z.C., Vergin, K., Mannenbach, C., Block, S., Yang, Q., Blainey, P., Carlson, C., and Giovannnoni, S. (2018) Optofluidic single-cell genome amplification of sub-micron bacteria in the ocean subsurface. Front. Microbiol. 9:1152. https://doi.org/10.3389/fmicb.2018.01152

Maas, A.E., Blanco-Bercial, L., Lo, A., Tarrant, A.M., and Timmins-Schiffman, E. (2018) Variations in copepod proteome and respiration rate in association with diel vertical migration and circadian cycle. Biol. Bull. 235(1): 30-42.

Warwick-Dugdale, J., Holger, H.B., Allen, M.J., and Temperton, B. (2019) Host-hijacking and planktonic piracy: how phages command the microbial high seas. Virology Journal 16(1):15.

Warwick-Dugdale, J., Solonenko, N., Moore, K., Chittick, L., Gregory, AC., Allen, MJ., Sullivan, MB., and Temperton, B. (2019) Long-read viral metagenomics captures abundant and microdiverse viral populations and their niche-defining genomic islands. PeerJ 7:e6800. http://doi.org/10.7717/peerj.6800

White, A.E., Giovannoni, S.J., Zhao, Y., Vergi, K., and Carlson, C.A. (2019) Elemental content and stoichiometry of SAR11 chemoheterotrophic marine bacteria. Limnology and Oceanography Letters 4(2): 44-51. https://doi.org/10.1002/lol2.10103

2018-2017 Funding Period
Giovannoni, SJ. (2017). SAR11 bacteria: the most abundant plankton in the oceans. Ann Rev Mar Sci 9: 231-55. https://doi.org/10.1146/annurev-marine-010814-015934

James, A.K., Passow, U., Brzezinski, M.A., Parsons, R.J., Trapani, J.N. and Carlson, C.A. (2017) Elevated pCO2 enhances bacterioplankton removal of organic carbonPloS One 12(3), p.e0173145.

Johnson, W.M., Kido Soule, M.C., and Kujawinski, E.B. (2017) Interpreting the impact of matrix on extraction efficiency and instrument response in a targeted metabolomics method. Limnol. Oceanogr. Methods 15(4): 417-428.

Landry, Z., Swan, B.K., Herndl, G.J., Stepanauskas, R., and Giovannoni, S.J. (2017) SAR202 genomes from the dark ocean predict pathways for the oxidation of recalcitrant dissolved organic matter. mBio 8(2) doi:10.1128/mBio.00413-17.

Roux, S., et. al. (2018) Minimum information about an uncultivated virus genome. Nature Biotechnology 37(1): 29-37.

Vergin, K.L., Jhirad, N., Dodge, J., Carlson, C.A., and Giovannoni, S.J. (2017) Marine bacterioplankton consortia follow deterministic, non-neutral community assembly rules. Aquat. Microb. Ecol. 79(2): 165-175.

Motivating Studies for BIOS-SCOPE
Carlson, C.A., Morris, R., Parsons, R., Treusch, A.H., Giovannoni, S.J., Vergin, K. (2009) Seasonal dynamics of SAR11 populations in the euphotic and mesopelagic zones of the northwestern Sargasso SeaThe ISME Journal 3: 283-295.

Carlson, C.A., Giovannoni, S.J., Hansell, D.A., Goldberg, S.J., Parsons, R., and Vergin K. (2004) Interactions among dissolved organic carbon, microbial processes, and community structure in the mesopelagic zone of the northwestern Sargasso Sea. Limnol. Oceanogr. 49(4): 1073-1083.

Carlson, C.A., Giovannoni, S.J., Hansell, D.A., Goldberg, S.J., Parsons, R., Otero, M.P., Vergin, K., and Wheeler, B.R. (2002) Effect of nutrient amendments on bacterioplankton production, community structure, and DOC utilization in the northwestern Sargasso Sea. Aquatic Microbial Ecology 30: 19-36.

Giovannoni, S., Vergin, K. and Carlson, C. (2014). Twenty-five years of omics at BATS. OCB News 7(1): 1-6.

Giovannoni, S.J. and Vergin, K.L. (2012) Seasonality in ocean microbial communities. Science 335: 671-676.

Giovannoni, S.J., Bibbs, L., Cho, J-C., Stapels, M.D., Desiderio, R., Vergin, K.L., Rappe, M.S., Laney, S., Wilhelm, L.J., Tripp, H.J., Mathur, E.J., Barofsky, D.F. (2005) Proteorhodopsin in the ubiquitous marine bacterium SAR11Nature 438(3): 82-85

Giovannoni, S.J., Tripp, H.J., Givan, S., Podar, M., Vergin, K.L., Baptista, D., Bibbs, L., Eads, J., Richardson, T.H., Noordewier, M., Rappe, M.S., Short, J.M., Carrington, J.C., Mathur, E.J. (2005) Genome streamlining in a cosmopolitan oceanic bacteriumScience 309: 1242-1245

Giovannoni, S. (2004) Oceans of bacteriaNature 430: 515-516

Goldberg, S.J., Carlson, C.A., Hansell, D.A., Nelson, N.B. and Siegel, D.A. (2009) Temporal dynamics of dissolved combined neutral sugars and the quality of dissolved organic matter in the Northwest Sargasso Sea. Deep-Sea Research I 56: 672-685.

Kujawinski EB, Longnecker K, Barott KL, Weber RJM, and Kido Soule MC. (2016) Microbial community structure affects marine dissolved organic matter composition. Frontiers in Marine Science 3: 1-15

Kujawinski EB (2011) The impact of microbial metabolism on marine dissolved organic matter. Annu Rev Mar Sci 3: 567-599.

Kujawinski EB, Longnecker K, Blough NV, Del Vecchio R, Finlay L, Kitner JB, and Giovannoni SJ. (2009) Identification of possible source markers in marine dissolved organic matter using ultrahigh resolution mass spectrometry. Geochim Cosmochim Acta 73: 4384-4399.

Kujawinski EB. (2002) Electrospray ionization Fourier transform ion cyclotron resonance mass spectrometry (ESI FT-ICR MS): characterization of complex environmental mixtures. Environmental Forensics 3: 207-216.

Morris, R.M., Rappe, M.S., Urbach, E., Connon, S.A., and Giovannoni, S.J. (2004) Prevalence of the Chlorfexi-related SAR202 bacterioplankton cluster throughout the mesopelagic zone and deep ocean. Applied and Environmental Microbiology 70(5): 2836-2842.

Morris, R.M., Rappe, M.S., Connon, S.A., Vergin, K.L., Siebold, W.A., Carlson, C.A., Giovannoni, S.J. (2002) SAR11 clade dominates ocean surface bacterioplankton communitiesNature 420: 806-810

Nelson, C.E., Carlson, C.A., Ewart, C.S., and Halewood, E.R. (2013) Community differentiation and population enrichment of Sargasso Sea bacterioplankton in the euphotic zone of a mesoscale mode-water eddy. Environmental Microbiology 16(3): 871-887. doi:10.1111/1462-2920.12241

Parsons, R.J., Breitbart, M., Lomas, M.W., Carlson, C. (2011) Ocean time-series reveals recurring seasonal patterns of virioplankton dynamics in the northwestern Sargasso SeaThe ISME Journal (August): 1-12.

Truesch, A.H., Demir-Hilton, E., Vergin, K.L., Worden, A.Z., Carlson, C.A., Donatz, M.G., Burton, R.M., and Giovannoni, S.J. (2012). Phytoplankton distribution patterns in the northwestern Sargasso Sea revealed by small subunit rRNA genes from plastids. The ISME Journal 6: 481-492.

Truesch, A.H., Vergin, K.L., Finlay, L.A., Donatz, M.G., Burton, R.M., Carlson, C.A. and Giovannoni, S.J. (2009) Seasonality and vertical structure of microbial communities in an ocean gyre. The ISME Journal 3(10): 1-16.

Vergin, K.L., Beszteri, B., Monier, A., Thrash, J.C., Temperton, B., Treusch, A.H., Kilpert, F., Worden, A.Z., and Giovannoni, S.J. (2013) High-resolution SAR11 ecotype dynamics at the Bermuda Atlantic Time-series Study site by phylogenetic placement of pyrosequences. The ISME Journal 7: 1322-1332.

Vergin, K.L., Done, B., Carlson, C.A. and Giovannoni, S.J. (2013) Spatiotemporal distributions of rare bacterioplankton populations indicate adaptive strategies in the oligotrophic ocean. Aquatic Microbial Ecology 71: 1-13.