Unifying chemical and biological perspectives of carbon accumulation in the environment

© 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.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

Transformations of carotenoids in the oceanic water column

Submitted in partial fulfillment of the requirements for the degree of Doctor of Philosophy at the Massachusetts Institute of Technology and the Woods Hole Oceanographic Institution August 1982In an effort to understand the more general mechanisms and rates of pre-depositional reactions that transform organic matter, the types and relevant time scales of reactions that transform carotenoid pigments in the oceanic water column were studied. Suspended particulate matter collected from surface waters of Buzzards Bay, Massachusetts and the Peru upwelling system has a carotenoid distribution reflecting the phytoplanktonic source of the material. The carotenoid distribution of sediment trap samples collected in these same areas was dominated by transformation products. Fucoxanthin, the primary carotenoid of marine diatoms, typically constituted 77-100% of the total fucopigments in suspended particulate material. In sediment trap samples this pigment constituted only 4-85% of the total. The remaining 15-96% of the pigments consisted of the fucoxanthin transformations products: free alcohols (2-94%), dehydrates (0-6%), and opened epoxides (0-19%). Preliminary results suggest that carotenoid esters are hydrolyzed to free alcohols at a rate determined by the turnover of primary productivity. The dehydrated and epoxide opened intermediates of fucoxanthin represent products of transformation reactions that operate over much longer time scales (0.1-10 yrs). Dehydration and epoxide opening are not significant water column transformations, but are important in surface sediments.This research was supported by the Ocean Sciences Section, National Science Foundation grants OCE 79-25352 and OCE 81-18436, the Office of Naval Research Contract N00014-74-Co-262NR 083-004, the Woods Hole Coastal Research Center project 25 000067 04, and a Woods Hole Oceanographic Institution Student Fellowship

An extended siderophore suite from Synechococcus sp. PCC 7002 revealed by LC-ICPMS-ESIMS

Author Posting. © The Author(s), 2015. This is the author's version of the work. It is posted here by permission of Royal Society of Chemistry for personal use, not for redistribution. The definitive version was published in Metallomics 7 (2015): 877-884, doi:10.1039/C5MT00005J.Siderophores are thought to play an important role in iron cycling in the ocean, but relatively few marine siderophores have been identified. Sensitive, high throughput methods hold promise for expediting the discovery and characterization of new siderophores produced by marine microbes. We developed a methodology for siderophore characterization that combines liquid chromatography (LC) inductively coupled plasma mass spectrometry (ICPMS) with high resolution electrospray ionization mass spectrometry (ESIMS). To demonstrate this approach, we investigated siderophore production by the marine cyanobacteria Synechococcus sp. PCC 7002. Three hydroxamate siderophores, synechobactin A-C, have been previously isolated and characterized from this strain. These compounds consist of an iron binding head group attached to a fatty acid side chain of variable length (C12, C10, and C8 respectively). In this study, we detected six iron-containing compounds in Synechococcus sp. PCC 7002 media by LC-ICPMS. To identify the molecular ions of these siderophores, we aligned the chromatographic retention times of peaks from the LC-ICPMS chromatogram with features detected from LC-ESIMS spectra using an algorithm designed to recognize metal isotope patterns. Three of these compounds corresponded to synechobactins A (614 m/z), B (586m/z), and C (558m/z). The MS2 spectra of these compounds revealed diagnostic synechobactin fragmentation patterns which were used to confirm the identity of the three unknown compounds (600, 628, and 642 m/z) as new members of the synechobactin suite with side chain lengths of 11, 13, and 14 carbons. These results demonstrate the potential of combined LCMS techniques for the identification of novel iron-organic complexes.This work was supported by the National Science Foundation program in Chemical Oceanography (OCE-1356747), and by the National Science Foundation Science and Technology Center for Microbial Oceanography Research and Education (C-MORE; DBI-0424599).2016-03-1

Reconstructing the phytoplankton community of the Cariaco Basin during the Younger Dryas cold event using chlorin steryl esters

Author Posting. © American Geophysical Union, 2004. This article is posted here by permission of American Geophysical Union for personal use, not for redistribution. The definitive version was published in Paleoceanography 19 (2004): PA01006, doi:10.1029/2003PA000907.A record of the downcore distribution of chlorin steryl esters (CSEs) through the Younger Dryas was produced from Cariaco Basin sediments in order to assess the potential use of CSEs as recorders of the structure of phytoplankton communities through time. Using an improved high-performance liquid chromatography method for the separation of CSEs, we find significant changes in the distribution of CSEs during the Younger Dryas in the Cariaco Basin. During the Younger Dryas, enhanced upwelling in the Cariaco Basin caused an increase in the diatom population and therefore an increase in the relative abundance of CSEs derived from diatoms. In contrast, the dinoflagellate population, and therefore CSEs derived from dinoflagellates, decreased in response to the climate change during the Younger Dryas. These community shifts agree well with the shifts observed in the present day on a seasonal basis that result from the north-south migration of the Intertropical Convergence Zone over the Cariaco Basin. We also identify changes in the abundance of several CSEs that seem to reflect rapid warming and cooling events. This study suggests that CSEs are useful proxies for reconstructing phytoplankton communities and paleoenvironments.This work was supported by the Chemical Oceanography Division of the National Science Foundation and a WHOI Watson Fellowship (to KAD)

Hidden cycle of dissolved organic carbon in the deep ocean

Marine dissolved organic carbon (DOC) is a large (660 Pg C) reactive carbon reservoir that mediates the oceanic microbial food web and interacts with climate on both short and long timescales. Carbon isotopic content provides information on the DOC source via δ[superscript 13]C and age via Δ[superscript 14]C. Bulk isotope measurements suggest a microbially sourced DOC reservoir with two distinct components of differing radiocarbon age. However, such measurements cannot determine internal dynamics and fluxes. Here we analyze serial oxidation experiments to quantify the isotopic diversity of DOC at an oligotrophic site in the central Pacific Ocean. Our results show diversity in both stable and radio isotopes at all depths, confirming DOC cycling hidden within bulk analyses. We confirm the presence of isotopically enriched, modern DOC cocycling with an isotopically depleted older fraction in the upper ocean. However, our results show that up to 30% of the deep DOC reservoir is modern and supported by a 1 Pg/y carbon flux, which is 10 times higher than inferred from bulk isotope measurements. Isotopically depleted material turns over at an apparent time scale of 30,000 y, which is far slower than indicated by bulk isotope measurements. These results are consistent with global DOC measurements and explain both the fluctuations in deep DOC concentration and the anomalous radiocarbon values of DOC in the Southern Ocean. Collectively these results provide an unprecedented view of the ways in which DOC moves through the marine carbon cycle.National Science Foundation (U.S.) (Grant OCE-0930866)National Science Foundation (U.S.) (Grant OCE-0930551

Dissolved organic matter in the ocean : a controversy stimulates new insights

Author Posting. © Oceanography Society, 2009. This article is posted here by permission of Oceanography Society for personal use, not for redistribution. The definitive version was published in Oceanography 22 no. 4 (2009): 202-211.Containing as much carbon as the atmosphere, marine dissolved organic matter is one of Earth’s major carbon reservoirs. With invigoration of scientific inquiries into the global carbon cycle, our ignorance of its role in ocean biogeochemistry became untenable. Rapid mobilization of relevant research two decades ago required the community to overcome early false leads, but subsequent progress in examining the global dynamics of this material has been steady. Continuous improvements in analytical skill coupled with global ocean hydrographic survey opportunities resulted in the generation of thousands of measurements throughout the major ocean basins. Here, observations and model results provide new insights into the large-scale variability of dissolved organic carbon, its contribution to the biological pump, and its deep ocean sinks.The US National Science Foundation supported this work under grants OCE 0752972 to DAH and CAC, OCE 0751733 and BIO 0792384 to DJR. The Gordon and Betty Moore Foundation also provided support to DJR

Phosphorus dynamics in biogeochemically distinct regions of the southeast subtropical Pacific Ocean

The southeast subtropical Pacific Ocean was sampled along a zonal transect between the coasts of Chile and Easter Island. This remote area of the world’s ocean presents strong gradients in physical (e.g., temperature, density and light), chemical (e.g., salinity and nutrient concentrations) and microbiological (e.g., cell abundances, biomass and specific growth rates) properties. The goal of this study was to describe the phosphorus (P) dynamics in three main ecosystems along this transect: the upwelling regime off the northern Chilean coast, the oligotrophic area associated with the southeast subtropical Pacific gyre and the transitional area in between these two biomes. We found that inorganic phosphate (Pi) concentrations were high and turnover times were long (>210 nmol l−1 and >31 d, respectively) in the upper water column, along the entire transect. Pi uptake rates in the gyre were low (euphotic layer integrated rates were 0.26 mmol m−2 d−1 in the gyre and 1.28 mmol m−2 d−1 in the upwelling region), yet not only driven by decreases in particle mass or cell abundance (particulate P- and cell- normalized Pi uptake rates in the euphotic layer were ∼1–4 times and ∼3–15 times lower in the gyre than in the upwelling, respectively). However these Pi uptake rates were at or near the maximum Pi uptake velocity (i.e., uptake rates in Pi amended samples were not significantly different from those at ambient concentration: 1.5 and 23.7 nmol l−1 d−1 at 50% PAR in the gyre and upwelling, respectively). Despite the apparent Pi replete conditions, selected dissolved organic P (DOP) compounds were readily hydrolyzed. Nucleotides were the most bioavailable of the DOP substrates tested. Microbes actively assimilated adenosine-5′-triphosphate (ATP) leading to Pi and adenosine incorporation as well as Pi release to the environment. The southeast subtropical Pacific Ocean is a Pi-sufficient environment, yet DOP hydrolytic processes are maintained and contribute to P-cycling across the wide range of environmental conditions present in this ecosystem

Revisiting the pink-red pigmented basidiomycete mirror yeast of the phyllosphere

© The Author(s), 2016. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in MicrobiologyOpen 5 (2016): 846–855, doi:10.1002/mbo3.374.By taking advantage of the ballistoconidium-forming capabilities of members of the genus Sporobolomyces, we recovered ten isolates from deciduous tree leaves collected from Vermont and Washington, USA. Analysis of the small subunit ribosomal RNA gene and the D1/D2 domain of the large subunit ribosomal RNA gene indicate that all isolates are closely related. Further analysis of their physiological attributes shows that all were similarly pigmented yeasts capable of growth under aerobic and microaerophilic conditions, all were tolerant of repeated freezing and thawing, minimally tolerant to elevated temperature and desiccation, and capable of growth in liquid or on solid media containing pectin or galacturonic acid. The scientific literature on ballistoconidium-forming yeasts indicates that they are a polyphyletic group. Isolates of Sporobolomyces from two geographically separated sites show almost identical phenotypic and physiological characteristics and a monophyly with a broad group of differently named Sporobolomyces/Sporidiobolus species based on both small subunit ribosomal RNA (SSU rRNA) and D1/D2 domains of the LSU rRNA gene sequences

Sampling of basement fluids via circulation obviation retrofit kits (CORKs) for dissolved gases, fluid fixation at the seafloor, and the characterization of organic carbon

© 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.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.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

Diversity and productivity of photosynthetic picoeukaryotes in biogeochemically distinct regions of the South East Pacific Ocean

© The Author(s), 2016. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Limnology and Oceanography 61 (2016): 806–824, doi:10.1002/lno.10255.Picophytoplankton, including photosynthetic picoeukaryotes (PPE) and unicellular cyanobacteria, are important contributors to plankton biomass and primary productivity. In this study, phytoplankton composition and rates of carbon fixation were examined across a large trophic gradient in the South East Pacific Ocean (SEP) using a suite of approaches: photosynthetic pigments, rates of 14C-primary productivity, and phylogenetic analyses of partial 18S rRNA genes PCR amplified and sequenced from flow cytometrically sorted cells. While phytoplankton >10 μm (diatoms and dinoflagellates) were prevalent in the upwelling region off the Chilean coast, picophytoplankton consistently accounted for 55–92% of the total chlorophyll a inventories and >60% of 14C-primary productivity throughout the sampling region. Estimates of rates of 14C-primary productivity derived from flow cytometric sorting of radiolabeled cells revealed that the contributions of PPE and Prochlorococcus to euphotic zone depth-integrated picoplankton productivity were nearly equivalent (ranging 36–57%) along the transect, with PPE comprising a larger share of picoplankton productivity than cyanobacteria in the well-lit (>15% surface irradiance) region compared with in the lower regions (1–7% surface irradiance) of the euphotic zone. 18S rRNA gene sequence analyses revealed the taxonomic identities of PPE; e.g., Mamiellophyceae (Ostreococcus) were the dominant PPE in the upwelling-influenced waters, while members of the Chrysophyceae, Prymnesiophyceae, Pelagophyceae, and Prasinophyceae Clades VII and IX flourished in the oligotrophic South Pacific Subtropical Gyre. Our results suggest that, despite low numerical abundance in comparison to cyanobacteria, diverse members of PPE are significant contributors to carbon cycling across biogeochemically distinct regions of the SEP.Support for this work derived from U.S. National Science Foundation grants to C-MORE (EF-0424599; DMK) and OCE-1241263 (MJC). Additional support was received from the University of Hawai'i Denise B. Evans Research Fellowship in Oceanography (YMR), the Gordon and Betty Moore Foundation (DMK), and the Simons Foundation via the Simons Collaboration on Ocean Processes and Ecology (SCOPE: DJR, MJC, and DMK)