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  • 1
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    Element-selective targeting of nutrient metabolites in environmental samples by inductively coupled plasma mass spectrometry and electrospray ionization mass spectrometry (2021)
    Frontiers Media
    Details
    Publication Date: 2022-10-26
    Description: © The Author(s), 2021. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Li, J., Boiteau, R. M., Babcock-Adams, L., Acker, M., Song, Z., McIlvin, M. R., & Repeta, D. J. Element-selective targeting of nutrient metabolites in environmental samples by inductively coupled plasma mass spectrometry and electrospray ionization mass spectrometry. Frontiers in Marine Science, 8, (2021): 630494, https://doi.org/10.3389/fmars.2021.630494.
    Description: Metabolites that incorporate elements other than carbon, nitrogen, hydrogen and oxygen can be selectively detected by inductively coupled mass spectrometry (ICPMS). When used in parallel with chromatographic separations and conventional electrospray ionization mass spectrometry (ESIMS), ICPMS allows the analyst to quickly find, characterize and identify target metabolites that carry nutrient elements (P, S, trace metals; “nutrient metabolites”), which are of particular interest to investigations of microbial biogeochemical cycles. This approach has been applied to the study of siderophores and other trace metal organic ligands in the ocean. The original method used mass search algorithms that relied on the ratio of stable isotopologues of iron, copper and nickel to assign mass spectra collected by ESIMS to metabolites carrying these elements detected by ICPMS. However, while isotopologue-based mass assignment algorithms were highly successful in characterizing metabolites that incorporate some trace metals, they do not realize the whole potential of the ICPMS/ESIMS approach as they cannot be used to assign the molecular ions of metabolites with monoisotopic elements or elements for which the ratio of stable isotopes is not known. Here we report a revised ICPMS/ESIMS method that incorporates a number of changes to the configuration of instrument hardware that improves sensitivity of the method by a factor of 4–5, and allows for more accurate quantitation of metabolites. We also describe a new suite of mass search algorithms that can find and characterize metabolites that carry monoisotopic elements. We used the new method to identify siderophores in a laboratory culture of Vibrio cyclitrophicus and a seawater sample collected in the North Pacific Ocean, and to assign molecular ions to monoisotopic cobalt and iodine nutrient metabolites in extracts of a laboratory culture of the marine cyanobacterium Prochorococcus MIT9215.
    Description: This work was generously supported by the National Science Foundation grant OCE-1829761 to RB and OCE-1356747 and -1736280 to DR. DR also received generous support from the Simons Foundation Life Sciences Project Award 49476.
    Keywords: LC-MS ; Algorithm ; Environmental metabolomics ; Trace metal ; Siderophores
    Repository Name: Woods Hole Open Access Server
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  • 2
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    Iron depletion in the deep chlorophyll maximum: mesoscale eddies as natural iron fertilization experiments (2022)
    American Geophysical Union
    Details
    Publication Date: 2022-10-26
    Description: © The Author(s), 2021. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Hawco, N. J., Barone, B., Church, M. J., Babcock-Adams, L., Repeta, D. J., Wear, E. K., Foreman, R. K., Bjorkman, K. M., Bent, S., Van Mooy, B. A. S., Sheyn, U., DeLong, E. F., Acker, M., Kelly, R. L., Nelson, A., Ranieri, J., Clemente, T. M., Karl, D. M., & John, S. G. Iron depletion in the deep chlorophyll maximum: mesoscale eddies as natural iron fertilization experiments. Global Biogeochemical Cycles, 35(12), (2021): e2021GB007112, https://doi.org/10.1029/2021GB007112.
    Description: In stratified oligotrophic waters, phytoplankton communities forming the deep chlorophyll maximum (DCM) are isolated from atmospheric iron sources above and remineralized iron sources below. Reduced supply leads to a minimum in dissolved iron (dFe) near 100 m, but it is unclear if iron limits growth at the DCM. Here, we propose that natural iron addition events occur regularly with the passage of mesoscale eddies, which alter the supply of dFe and other nutrients relative to the availability of light, and can be used to test for iron limitation at the DCM. This framework is applied to two eddies sampled in the North Pacific Subtropical Gyre. Observations in an anticyclonic eddy center indicated downwelling of iron-rich surface waters, leading to increased dFe at the DCM but no increase in productivity. In contrast, uplift of isopycnals within a cyclonic eddy center increased supply of both nitrate and dFe to the DCM, and led to dominance of picoeukaryotic phytoplankton. Iron addition experiments did not increase productivity in either eddy, but significant enhancement of leucine incorporation in the light was observed in the cyclonic eddy, a potential indicator of iron stress among Prochlorococcus. Rapid cycling of siderophores and low dFe:nitrate uptake ratios also indicate that a portion of the microbial community was stressed by low iron. However, near-complete nitrate drawdown in this eddy, which represents an extreme case in nutrient supply compared to nearby Hawaii Ocean Time-series observations, suggests that recycling of dFe in oligotrophic ecosystems is sufficient to avoid iron limitation in the DCM under typical conditions.
    Description: The expedition and analyses were supported by the Simons Foundation SCOPE Grant 329108 to S. G. John, M. J. Church, D. J. Repeta, B. Van Mooy, E. F. DeLong, and D. M. Karl. N. J. Hawco was supported by a Simons Foundation Marine Microbial Ecology and Evolution postdoctoral fellowship (602538) and Simons Foundation grant 823167.
    Keywords: Chlorophyll ; Photosynthesis ; Iron limitation ; Oligotrophic ; Prochlorococcus ; Eddies
    Repository Name: Woods Hole Open Access Server
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  • 3
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    Discovery of chlorophyll d: isolation and characterization of a far-red cyanobacterium from the original site of manning and strain (1943) at Moss Beach, California (2022)
    MDPI
    Details
    Publication Date: 2022-10-26
    Description: © The Author(s), 2022. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Kiang, N. Y., Swingley, W. D., Gautam, D., Broddrick, J. T., Repeta, D. J., Stolz, J. F., Blankenship, R. E., Wolf, B. M., Detweiler, A. M., Miller, K. A., Schladweiler, J. J., Lindeman, R., & Parenteau, M. N. Discovery of chlorophyll d: isolation and characterization of a far-red cyanobacterium from the original site of manning and strain (1943) at Moss Beach, California. Microorganisms, 10(4), (2022): 819, https://doi.org/10.3390/microorganisms10040819.
    Description: We have isolated a chlorophyll-d-containing cyanobacterium from the intertidal field site at Moss Beach, on the coast of Central California, USA, where Manning and Strain (1943) originally discovered this far-red chlorophyll. Here, we present the cyanobacterium’s environmental description, culturing procedure, pigment composition, ultrastructure, and full genome sequence. Among cultures of far-red cyanobacteria obtained from red algae from the same site, this strain was an epiphyte on a brown macroalgae. Its Qyin vivo absorbance peak is centered at 704–705 nm, the shortest wavelength observed thus far among the various known Acaryochloris strains. Its Chl a/Chl d ratio was 0.01, with Chl d accounting for 99% of the total Chl d and Chl a mass. TEM imagery indicates the absence of phycobilisomes, corroborated by both pigment spectra and genome analysis. The Moss Beach strain codes for only a single set of genes for producing allophycocyanin. Genomic sequencing yielded a 7.25 Mbp circular chromosome and 10 circular plasmids ranging from 16 kbp to 394 kbp. We have determined that this strain shares high similarity with strain S15, an epiphyte of red algae, while its distinct gene complement and ecological niche suggest that this strain could be the closest known relative to the original Chl d source of Manning and Strain (1943). The Moss Beach strain is designated Acaryochloris sp. (marina) strain Moss Beach.
    Description: N.Y.K., M.N.P. and R.E.B. were supported by the NASA Virtual Planetary Laboratory team (VPL), which was funded under NASA Astrobiology Institute Cooperative Agreement Number NNA13AA93A, and Grant Number 80NSSC18K0829. This work also benefited from participation in the NASA Nexus for Exoplanet Systems Science (NExSS) research coordination network (RCN). W.D.S, N.Y.K. and M.N.P. were also supported by a NASA Exobiology grant No. 80NSSC19K0478. J.TB. was supported by the NASA Postdoctoral Program (NPP) award number NPP168014S. N.Y.K. received training support from the NASA Goddard Space Flight Center Training Office to take the Microbial Diversity course at the Marine Biological Laboratory, Woods Hole, MA, USA.
    Keywords: Chlorophyll d ; Acaryochloris ; Moss Beach ; Cyanobacteria ; Far-red photosynthesis ; Photosynthetic pigments ; Absorbance spectra ; Genome sequence
    Repository Name: Woods Hole Open Access Server
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  • 4
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    Bacterial quorum-sensing signal arrests phytoplankton cell division and impacts virus-induced mortality (2021)
    American Society for Microbiology
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    Publication Date: 2022-05-27
    Description: © The Author(s), 2021. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Pollara, S. B., Becker, J. W., Nunn, B. L., Boiteau, R., Repeta, D., Mudge, M. C., Downing, G., Chase, D., Harvey, E. L., & Whalen, K. E. Bacterial quorum-sensing signal arrests phytoplankton cell division and impacts virus-induced mortality. Msphere, 6(3), (2021): e00009-21, https://doi.org/10.1128/mSphere.00009-21.
    Description: Interactions between phytoplankton and heterotrophic bacteria fundamentally shape marine ecosystems by controlling primary production, structuring marine food webs, mediating carbon export, and influencing global climate. Phytoplankton-bacterium interactions are facilitated by secreted compounds; however, linking these chemical signals, their mechanisms of action, and their resultant ecological consequences remains a fundamental challenge. The bacterial quorum-sensing signal 2-heptyl-4-quinolone (HHQ) induces immediate, yet reversible, cellular stasis (no cell division or mortality) in the coccolithophore Emiliania huxleyi; however, the mechanism responsible remains unknown. Using transcriptomic and proteomic approaches in combination with diagnostic biochemical and fluorescent cell-based assays, we show that HHQ exposure leads to prolonged S-phase arrest in phytoplankton coincident with the accumulation of DNA damage and a lack of repair despite the induction of the DNA damage response (DDR). While this effect is reversible, HHQ-exposed phytoplankton were also protected from viral mortality, ascribing a new role of quorum-sensing signals in regulating multitrophic interactions. Furthermore, our data demonstrate that in situ measurements of HHQ coincide with areas of enhanced micro- and nanoplankton biomass. Our results suggest bacterial communication signals as emerging players that may be one of the contributing factors that help structure complex microbial communities throughout the ocean.
    Description: Funding for this work was supported by an NSF grant (OCE-1657808) awarded to K.E.W. and E.L.H. K.E.W. was also supported by a faculty research grant from Haverford College as well as funding from the Koshland Integrated Natural Science Center and Green Fund at Haverford College. E.L.H. was also supported by a Sloan Foundation research fellowship. B.L.N. was supported by an NSF grant (OCE-1633939). M.C.M. was supported by an NIH training grant (T32 HG000035). Mass spectrometry was partially supported by the University of Washington Proteomics Resource (UWPR95794). D.R. was supported by funding through the Gordon and Betty Moore Foundation (grant 6000), a Simons Collaboration for Ocean Processes and Ecology grant (329108), and an NSF grant (OCE-1736280). R.B. was supported by an NSF graduate research fellowship and an NSF grant (OCE-1829761).
    Repository Name: Woods Hole Open Access Server
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  • 5
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    Phosphonate production by marine microbes: exploring new sources and potential function (2022)
    National Academy of Sciences
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    Publication Date: 2022-06-10
    Description: © The Author(s), 2022. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Acker, M., Hogle, S. L., Berube, P. M., Hackl, T., Coe, A., Stepanauskas, R., Chisholm, S. W., & Repeta, D. J. Phosphonate production by marine microbes: exploring new sources and potential function. Proceedings of the National Academy of Sciences of the United States of America, 119(11), (2022): e2113386119, https://doi.org/10.1073/pnas.2113386119.
    Description: Phosphonates are organophosphorus metabolites with a characteristic C-P bond. They are ubiquitous in the marine environment, their degradation broadly supports ecosystem productivity, and they are key components of the marine phosphorus (P) cycle. However, the microbial producers that sustain the large oceanic inventory of phosphonates as well as the physiological and ecological roles of phosphonates are enigmatic. Here, we show that phosphonate synthesis genes are rare but widely distributed among diverse bacteria and archaea, including Prochlorococcus and SAR11, the two major groups of bacteria in the ocean. In addition, we show that Prochlorococcus can allocate over 40% of its total cellular P-quota toward phosphonate production. However, we find no evidence that Prochlorococcus uses phosphonates for surplus P storage, and nearly all producer genomes lack the genes necessary to degrade and assimilate phosphonates. Instead, we postulate that phosphonates are associated with cell-surface glycoproteins, suggesting that phosphonates mediate ecological interactions between the cell and its surrounding environment. Our findings indicate that the oligotrophic surface ocean phosphonate pool is sustained by a relatively small fraction of the bacterioplankton cells allocating a significant portion of their P quotas toward secondary metabolism and away from growth and reproduction.
    Description: This work was supported in part by grants from the NSF (OCE-1153588 and DBI-0424599 to S.W.C.; OCE-1335810 and OIA-1826734 to R.S.; and OCE-1634080 to D.J.R.), the Gordon and Betty Moore Foundation (no. 6000 to D.J.R.), and the Simons Foundation (Life Sciences Project Award IDs 337262 and 647135 to S.W.C.; 510023 to R.S.; and Simons Collaboration on Ocean Processes and Ecology [SCOPE] Award ID 329108 to S.W.C. and D.J.R.).
    Keywords: phosphonate ; Prochlorococcus ; marine ; biogeochemistry ; phosphorus
    Repository Name: Woods Hole Open Access Server
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  • 6
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    Phosphonate cycling supports methane and ethylene supersaturation in the phosphate-depleted western North Atlantic Ocean (2020)
    Wiley
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    Publication Date: 2022-05-26
    Description: © The Author(s), 2020. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Sosa, O. A., Burrell, T. J., Wilson, S. T., Foreman, R. K., Karl, D. M., & Repeta, D. J. Phosphonate cycling supports methane and ethylene supersaturation in the phosphate-depleted western North Atlantic Ocean. Limnology and Oceanography, (2020), doi:10.1002/lno.11463.
    Description: In oligotrophic ocean regions, dissolved organic phosphorus (DOP) plays a prominent role as a source of phosphorus (P) to microorganisms. An important bioavailable component of DOP is phosphonates, organophosphorus compounds with a carbon‐phosphorus (C‐P) bond, which are ubiquitous in high molecular weight dissolved organic matter (HMWDOM). In addition to being a source of P, the degradation of phosphonates by the bacterial C‐P lyase enzymatic pathway causes the release of trace hydrocarbon gases relevant to climate and atmospheric chemistry. In this study, we investigated the roles of phosphate and phosphonate cycling in the production of methane (CH4) and ethylene (C2H4) in the western North Atlantic Ocean, a region that features a transition in phosphate concentrations from coastal to open ocean waters. We observed an inverse relationship between phosphate and the saturation state of CH4 and C2H4 in the water column, and between phosphate and the relative abundance of the C‐P lyase marker gene phnJ . In phosphate‐depleted waters, methylphosphonate and 2‐hydroxyethylphosphonate, the C‐P lyase substrates that yield CH4 and C2H4, respectively, were readily degraded in proportions consistent with their abundance and bioavailability in HMWDOM and with the concentrations of CH4 and C2H4 in the water column. We conclude that phosphonate degradation through the C‐P lyase pathway is an important source and a common production pathway of CH4 and C2H4 in the phosphate‐depleted surface waters of the western North Atlantic Ocean and that phosphate concentration can be an important control on the saturation state of these gases in the upper ocean.
    Description: We thank the captain and crew of the R/V Neil Armstrong and chief scientist Benjamin Van Mooy for supporting and leading research at sea. Chiara Santinelli and Eric Grabowski provided analyses of dissolved organic carbon. This research was funded by NSF Chemical Oceanography award OCE‐1634080 to D.J.R. Additional support was provided by the Gordon and Betty Moore Foundation grant 3794 to D.M.K. and grant 6000 to D.J.R., and the Simons Collaboration on Ocean Processes and Ecology (SCOPE) program grant 329108 to D.M.K., E.F.D., and D.J.R.
    Repository Name: Woods Hole Open Access Server
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  • 7
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    Sampling of basement fluids via circulation obviation retrofit kits (CORKs) for dissolved gases, fluid fixation at the seafloor, and the characterization of organic carbon (2020)
    Elsevier
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    Publication Date: 2022-05-26
    Description: © The Author(s), 2020. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Lin, H. T., Hsieh, C. C., Repeta, D. J., & Rappé, M. S. Sampling of basement fluids via circulation obviation retrofit kits (CORKs) for dissolved gases, fluid fixation at the seafloor, and the characterization of organic carbon. Methodsx, 7, (2020): 101033, doi:10.1016/j.mex.2020.101033.
    Description: The advanced instrumented GeoMICROBE sleds (Cowen et al., 2012) facilitate the collection of hydrothermal fluids and suspended particles in the subseafloor (basaltic) basement through Circulation Obviation Retrofit Kits (CORKs) installed within boreholes of the Integrated Ocean Drilling Program. The main components of the GeoMICROBE can be converted into a mobile pumping system (MPS) that is installed on the front basket of a submersible or remotely-operated-vehicle (ROV). Here, we provide details of a hydrothermal fluid-trap used on the MPS, through which a gastight sampler can withdraw fluids. We also applied the MPS to demonstrate the value of fixing samples at the seafloor in order to determine redox-sensitive dissolved iron concentrations and speciation measurements. To make the best use of the GeoMICROBE sleds, we describe a miniature and mobile version of the GeoMICROBE sled, which permits rapid turn-over and is relatively easy for preparation and operation. Similar to GeoMICROBE sleds, the Mobile GeoMICROBE (MGM) is capable of collecting fluid samples, filtration of suspended particles, and extraction of organics. We validate this approach by demonstrating the seafloor extraction of hydrophobic organics from a large volume (247L) of hydrothermal fluids. • We describe the design of a hydrothermal fluid-trap for use with a gastight sampler, as well as the use of seafloor fixation, through ROV- or submersible assisted mobile pumping systems. • We describe the design of a Mobile GeoMICROBE (MGM) that enhances large volume hydrothermal fluid sampling, suspended particle filtration, and organic matter extraction on the seafloor. • We provide an example of organic matter extracted and characterized from hydrothermal fluids via a MGM.
    Description: We dedicate this work to Dr. James P. Cowen, who had envisioned and constructed the integrated instrumentation, GeoMICROBE, to monitor the sub-basement biosphere. We thank the chief scientists, captains, crews, and science teams on board R/V Atlantis cruises AT15-35, AT15-51, AT15-66, AT18-07, MSM20-5, AT26-03, and AT26-18, and the pilots and crews of ROV Jason II and HOV Alvin. We thank our student assistants, Natalie Hamada, Kathryn Hu, Ryan Matzumoto, Everette Omori, and Fan-Chieh Chuang. This work was supported by the National Science Foundation-Microbial Observatory Project (NSF-MCB06-04014 to J. P. Cowen), Center for Dark Energy Biosphere Investigations (C-DEBI; NSF award OCE-0939564 to M. S. Rappé), NSF award OCE-1260723 (to M. S. Rappé), and the Ministry of Science and Technology of Taiwan award (MOST 105-2119-M-002-034, MOST 107-2611-M-002-002, MOST 108-2611-M-002-006, and MOST109-2611-M-002-008 to H.-T. Lin). Ministry of Education (MOE) Republic of China (Taiwan) 109L892601 to H.-T. Lin. NSF award OCE-1634080 (to D. J. Repeta), the Simons Foundation-Simons Collaboration on Ocean Processes and Ecology (SCOPE) award 329108 (to D. J. Repeta), the Gordon and Betty Moore Foundation award 6000 (to D. J. Repeta). This paper is SOEST contribution number 11121, HIMB contribution 1804 and C-DEBI contribution number 543.
    Keywords: GeoMICROBE ; Hydrothermal fluid ; Crustal fluid ; Mobile pumping system ; Helium ; Methane ; Dissolved organic matter ; Extraction and preconcentration ; Deep subseafloor
    Repository Name: Woods Hole Open Access Server
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  • 8
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    Unifying chemical and biological perspectives of carbon accumulation in the environment (2021)
    National Academy of Sciences
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    Publication Date: 2022-05-27
    Description: © The Author(s), 2021. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Repeta, D. J. Unifying chemical and biological perspectives of carbon accumulation in the environment. Proceedings of the National Academy of Sciences of the United States of America, 118(11), (2021); e2100935118, https://doi.org/10.1073/pnas.2100935118.
    Description: Heterotrophic microorganisms are fiendishly clever at degrading all shapes and sizes of organic compounds to extract the energy they need to build biomass. Every year marine phytoplankton fix ∼50 billion tons of carbon dioxide into organic matter, and every year marine heterotrophs respire nearly all of this organic matter back to carbon dioxide (1). Nearly all, but not all. With each spin of this carbon cycle, a small amount of organic matter escapes respiration and becomes sequestered in seawater, sediments, and soils. Over time, this small “leak” in the system leads to the accumulation of a vast reservoir of carbon; some 5 × 1019 kg of organic matter are thought to be sequestered in sedimentary rocks (2). This carbon sequestration has immense consequences for life on Earth, as illustrated by the change in climate we are now experiencing due in part to the transfer of a minute portion of this inventory from geologic reservoirs into the atmosphere.
    Repository Name: Woods Hole Open Access Server
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