Award Abstract # 1736772
A mechanistic microbial underpinning for the size-reactivity continuum of dissolved organic carbon degradation

NSF Org: OCE
Division Of Ocean Sciences
Recipient: UNIVERSITY OF NORTH CAROLINA AT CHAPEL HILL
Initial Amendment Date: June 26, 2017
Latest Amendment Date: May 19, 2021
Award Number: 1736772
Award Instrument: Standard Grant
Program Manager: Henrietta Edmonds
hedmonds@nsf.gov
 (703)292-7427
OCE
 Division Of Ocean Sciences
GEO
 Directorate For Geosciences
Start Date: September 1, 2017
End Date: August 31, 2022 (Estimated)
Total Intended Award Amount: $598,359.00
Total Awarded Amount to Date: $660,522.00
Funds Obligated to Date: FY 2017 = $598,359.00
FY 2021 = $62,163.00
History of Investigator:
  • Carol Arnosti (Principal Investigator)
    arnosti@email.unc.edu
Recipient Sponsored Research Office: University of North Carolina at Chapel Hill
104 AIRPORT DR STE 2200
CHAPEL HILL
NC  US  27599-5023
(919)966-3411
Sponsor Congressional District: 04
Primary Place of Performance: University of North Carolina at Chapel Hill
NC  US  27599-3300
Primary Place of Performance
Congressional District:
04
Unique Entity Identifier (UEI): D3LHU66KBLD5
Parent UEI:
NSF Program(s): Chemical Oceanography
Primary Program Source: 01001718DB NSF RESEARCH & RELATED ACTIVIT
01002122DB NSF RESEARCH & RELATED ACTIVIT
Program Reference Code(s): 097Z, 102Z, 1389
Program Element Code(s): 1670
Award Agency Code: 4900
Fund Agency Code: 4900
Assistance Listing Number(s): 47.050

ABSTRACT

Marine dissolved organic matter (DOM) is one of the largest actively-cycling reservoirs of organic carbon on the planet, and thus a major component of the global carbon cycle. The high molecular weight (HMW) fraction of DOM is younger in age and more readily consumed by microbes than lower molecular weight (LMW) fractions of DOM, but the reasons for this difference in reactivity between HMW DOM and LMW DOM are unknown. Two factors may account for the greater reactivity of HMW DOM: (i) targeted uptake of HMW DOM by specific bacteria, a process the PI and her collaborators at the Max Planck Institute for Marine Microbiology (MPI) recently identified in surface ocean waters; and (ii) a greater tendency of HMW DOM to aggregate and form gels and particles, which can be colonized by bacteria that are well-equipped to breakdown organic matter. Scientists and students from the University of North Carolina (UNC) - Chapel Hill will collaborate with researchers at the MPI for Marine Microbiology (Bremen, Germany) to investigate this breakdown of HMW DOM by marine microbial communities. These investigations will include a field expedition in the North Atlantic, during which HMW DOM degradation rates and patterns will be compared in different water masses and under differing conditions of organic matter availability. DOM aggregation potential, and degradation rates of these aggregates, will also be assessed. Specialized microscopy will be used in order to pinpoint HMW DOM uptake mechanisms and rates. The work will be complemented by ongoing studies of specific bacteria that breakdown HMW DOM, their genes, and their proteins. Graduate as well as undergraduate students will participate as integral members of the research team in all aspects of the laboratory and field work; aspects of the project will also be integrated into classes the scientist teaches at UNC.

The existence of a size-reactivity continuum of DOM - observations and measurements showing that HMW DOM tends to be younger and more reactive than lower MW DOM ? has been demonstrated in laboratory and field investigations in different parts of the ocean. A mechanistic explanation for the greater reactivity of HMW DOM has been lacking, however. This project will investigate the mechanisms and measure rates of HMW DOM degradation, focusing on identifying the actors and determining the factors that contribute to rapid cycling of HMW DOM. Collaborative work at UNC and MPI-Bremen recently identified a new mechanism of HMW substrate uptake common among pelagic marine bacteria: these bacteria rapidly bind, partially hydrolyze, and transport directly across the outer membrane large fragments of HMW substrates that can then be degraded within the periplasmic space, avoiding production of LMW DOM in the external environment. This mode of substrate processing has been termed selfish, since targeted HMW substrate uptake sequesters resources away from other members of microbial communities. Measurements and models thus must account for three modes of substrate utilization in the ocean: selfish, sharing (external hydrolysis, leading to low molecular weight products), and scavenging (uptake of low molecular weight hydrolysis products without production of extracellular enzymes). Using field studies as well as mesocosm experiments, the research team will investigate the circumstances and locations at which different modes of substrate uptake predominate. A second focal point of the project is to determine the aggregation potential and microbial degradation of aggregated HMW DOM. Preliminary studies have demonstrated that particle-associated microbial communities utilize a broader range of enzymatic capabilities than their free-living counterparts. These capabilities equip particle-associated communities to effectively target a broad range of complex substrates. The project will thus focus on two key aspects of HMW DOM - the abilities of specialized bacteria to selectively sequester HMW substrates, as well as the greater potential of HMW substrates to aggregate ? and will quantify these factors at different locations and depths in the ocean. The project will thereby provide a mechanistic underpinning for observations of the DOC size-reactivity continuum, an essential part of developing an overall mechanistic understanding of organic matter degradation in the ocean.

PUBLICATIONS PRODUCED AS A RESULT OF THIS RESEARCH

Note:  When clicking on a Digital Object Identifier (DOI) number, you will be taken to an external site maintained by the publisher. Some full text articles may not yet be available without a charge during the embargo (administrative interval).

Some links on this page may take you to non-federal websites. Their policies may differ from this site.

(Showing: 1 - 10 of 23)
Hoarfrost, Adrienne and Brown, Nick and Brown, C. Titus and Arnosti, Carol and Wren, ed., Jonathan "Sequencing data discovery with MetaSeek" Bioinformatics , v.35 , 2019 https://doi.org/10.1093/bioinformatics/btz499 Citation Details
Manna, Vincenzo and Zoccarato, Luca and Banchi, Elisa and Arnosti, Carol and Grossart, Hans?Peter and Celussi, Mauro "Linking lifestyle and foraging strategies of marine bacteria: selfish behaviour of particle?attached bacteria in the northern Adriatic Sea" Environmental Microbiology Reports , 2022 https://doi.org/10.1111/1758-2229.13059 Citation Details
Lloyd, C. Chad and Brown, Sarah and Balmonte, John Paul and Hoarfrost, Adrienne and Ghobrial, Sherif and Arnosti, Carol "Particles act as ?specialty centers? with expanded enzymatic function throughout the water column in the western North Atlantic" Frontiers in Microbiology , v.13 , 2022 https://doi.org/10.3389/fmicb.2022.882333 Citation Details
Arnosti, C. and Reintjes, G. and Amann, R. "A mechanistic microbial underpinning for the size-reactivity continuum of dissolved organic carbon degradation" Marine Chemistry , v.206 , 2018 10.1016/j.marchem.2018.09.008 Citation Details
Balmonte, John Paul and Hasler?Sheetal, Harald and Glud, Ronnie N. and Andersen, Thorbjørn J. and Sejr, Mikael K. and Middelboe, Mathias and Teske, Andreas and Arnosti, Carol "Sharp contrasts between freshwater and marine microbial enzymatic capabilities, community composition, and DOM pools in a NE Greenland fjord" Limnology and Oceanography , v.65 , 2019 https://doi.org/10.1002/lno.11253 Citation Details
Bullock, Avery and Ziervogel, Kai and Ghobrial, Sherif and Smith, Shannon and McKee, Brent and Arnosti, Carol "A Multi-season Investigation of Microbial Extracellular Enzyme Activities in Two Temperate Coastal North Carolina Rivers: Evidence of Spatial but Not Seasonal Patterns" Frontiers in Microbiology , v.8 , 2017 10.3389/fmicb.2017.02589 Citation Details
Klassen, Leeann and Reintjes, Greta and Tingley, Jeffrey P. and Jones, Darryl R. and Hehemann, Jan-Hendrik and Smith, Adam D. and Schwinghamer, Timothy D. and Arnosti, Carol and Jin, Long and Alexander, Trevor W. and Amundsen, Carolyn and Thomas, Dallas a "Quantifying fluorescent glycan uptake to elucidate strain-level variability in foraging behaviors of rumen bacteria" Microbiome , v.9 , 2021 https://doi.org/10.1186/s40168-020-00975-x Citation Details
Hoarfrost, Adrienne and Nayfach, Stephen and Ladau, Joshua and Yooseph, Shibu and Arnosti, Carol and Dupont, Chris L. and Pollard, Katherine S. "Global ecotypes in the ubiquitous marine clade SAR86" The ISME Journal , v.14 , 2019 https://doi.org/10.1038/s41396-019-0516-7 Citation Details
Arnosti, Carol and Hinrichs, Kai-Uwe and Coffinet, Sarah and Wilkes, Heinz and Pantoja, Silvio "The Enduring Questions: What's for Dinner? Where's My Knife? ?and Can I Use My Fingers? (Unanswered) Questions Related to Organic Matter and Microbes in Marine Sediments" Frontiers in Marine Science , v.6 , 2019 10.3389/fmars.2019.00629 Citation Details
Arnosti, Carol and Hoarfrost, Adrienne and Balmonte, John Paul and Lloyd, C. Chad and Brown, Sarah A. and Ghobrial, Sherif "Empirical Definition of the Mad Buckets Magic Number: A Guide for Seagoing Scientists" Limnology and Oceanography Bulletin , v.32 , 2023 https://doi.org/10.1002/lob.10577 Citation Details
Traving, Sachia J. and Balmonte, John Paul and Seale, Dan and Arnosti, Carol and Glud, Ronnie N. and Hallam, Steven J. and Middelboe, Mathias "On Single-Cell Enzyme Assays in Marine Microbial Ecology and Biogeochemistry" Frontiers in Marine Science , v.9 , 2022 https://doi.org/10.3389/fmars.2022.846656 Citation Details
(Showing: 1 - 10 of 23)

PROJECT OUTCOMES REPORT

Disclaimer

This Project Outcomes Report for the General Public is displayed verbatim as submitted by the Principal Investigator (PI) for this award. Any opinions, findings, and conclusions or recommendations expressed in this Report are those of the PI and do not necessarily reflect the views of the National Science Foundation; NSF has not approved or endorsed its content.

 

Dissolved organic carbon in the ocean is one of the largest and biologically most active carbon reservoirs on earth. A considerable fraction of the dissolved organic carbon pool consists of large molecules (high molecular weight organic carbon). This high molecular weight carbon is known to be fresher and more biologically reactive than the rest of the dissolved organic carbon pool, but the reasons for higher biological reactivity were unknown. This project focused specifically on the mechanisms by which bacteria process and transform high molecular weight polysaccharides, a major part of the high molecular weight dissolved organic carbon pool. Polysaccharides are too large to be eaten directly by bacteria; instead, they must first be cut to smaller sizes before uptake. Typically, the polysaccharides are cut to smaller pieces outside the cell by enzymes (termed external hydrolysis); the resulting smaller pieces of organic carbon can be taken up by the organism that produced the enzymes, as well as by other bacteria that did not produce enzymes.

We discovered an addition mechanism of polysaccharide processing: some members of bacterial communities can bind, cut, and take up high molecular weight polysaccharides without losing pieces of organic matter to the external environment (referred to as a  selfish mechanism of uptake). Using a selfish uptake mechanism essentially guarantees a payback for the investment in the enzymes used to bind and cut their target food. As part of this project, we compared the rates and types of substrates processed via selfish uptake and external hydrolysis in different parts of the ocean. We expected the selfish mechanism to be used by specific bacteria that are relatively common in the upper ocean, in locations where much fresh organic matter is produced. Much to our surprise, we found that selfish uptake is found not only in the surface ocean, but also in the deep ocean. Furthermore, some highly complex organic matter that otherwise is untouched in the deep ocean is apparently processed only by selfish mechanisms. Rapid selfish uptake of high molecular weight organic carbon appears to be quite widespread in the ocean, carried out by a broad range of different types of bacteria: this mechanism is not restricted to a few types of organisms.

These findings are important because bacteria consume and transform much of the organic matter produced in the ocean. Understanding the mechanisms by which bacteria consume organic matter, and the factors controlling which organic matter is eaten in any given location, helps explain the ecology of bacterial communities that process organic matter, as well as the distribution of organic carbon in the ocean, and thus is central to the workings of the global carbon cycle. The ecological insights and methods refined as part of this project to identify specific bacteria that selfishly take up polysaccharides have implications far beyond the field of oceanography: bacterial communities in the guts of living organisms are essential to digestive processes. The technical approaches developed and refined in this project are already being applied also in biomedicine and veterinary studies.

 


 


Last Modified: 12/31/2022
Modified by: Carol Arnosti

Please report errors in award information by writing to: awardsearch@nsf.gov.

Print this page

Back to Top of page