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Research Spending & Results

Award Detail

Awardee:BIGELOW LABORATORY FOR OCEAN SCIENCES
Doing Business As Name:Bigelow Laboratory for Ocean Sciences
PD/PI:
  • Ramunas Stepanauskas
  • (207) 315-2567
  • rstepanauskas@bigelow.org
Award Date:09/15/2012
Estimated Total Award Amount: $ 900,000
Funds Obligated to Date: $ 900,000
  • FY 2012=$900,000
Start Date:09/01/2012
End Date:08/31/2016
Transaction Type:Grant
Agency:NSF
Awarding Agency Code:4900
Funding Agency Code:4900
CFDA Number:47.050
Primary Program Source:040100 NSF RESEARCH & RELATED ACTIVIT
Award Title or Description:Ocean's dark energy: Global inventory of chemoautotrophs in the aphotic realm
Federal Award ID Number:1232982
DUNS ID:077474757
Program:BIOLOGICAL OCEANOGRAPHY

Awardee Location

Street:60 Bigelow Drive
City:East Boothbay
State:ME
ZIP:04544-0380
County:East Boothbay
Country:US
Awardee Cong. District:01

Primary Place of Performance

Organization Name:Bigelow Laboratory for Ocean Sciences
Street:180 McKown Point Rd.
City:West Boothbay Harbor
State:ME
ZIP:04575-0475
County:West Boothbay Harbor
Country:US
Cong. District:01

Abstract at Time of Award

The dark ocean, defined as the water column below the photic, contains one of the largest microbial biomes on earth, composed of active and metabolically diverse microorganisms. These biota impact local processes and the global carbon cycling, e.g. by conducting a large fraction of marine organic matter remineralization. An increasing body of evidence suggests that chemoautotrophy in the dark ocean may also be significant, with potentially major implications to the dark ocean's microbial ecology and biogeochemistry. However, it remains largely unanswered what energy sources and metabolic pathways are used to support this microbial-driven dark carbon fixation and which microbial taxonomic groups possess chemoautotrophic metabolic pathways in the dark ocean. Intellectual Merit. The overall goal of this project is to obtain a comprehensive, global inventory of chemoautotrophs in the dark ocean through large-scale microbial single cell genomics, supplemented with metagenomic and metatranscriptomic sequencing. The investigators will address the following general hypotheses: 1. Multiple prokaryote taxonomic groups found in the dark ocean contain chemoautotrophic metabolic pathways. 2. Both known and previously unrecognized chemoautotrophy pathways are present in dark ocean's prokaryotes. 3. Dark ocean chemoautotrophs are broadly distributed around the globe, with biogeographic patterns determined by the isopycnal movement of water masses, water mass age, and the downward flux of organic matter. 4. Diverse chemoautotrophy pathways are expressed in the dark ocean. During the course of the project, single amplified genomes (SAGs) will be generated from all major intermediate and deep water masses around the globe, representing all major taxonomic groups of bacteria and archaea that are known to be present in the dark ocean. These SAGs will be analyzed for specific chemoautotrophy-indicative genes. Whole genome sequencing will be performed on a subset of SAGs, enabling detailed annotation of chemoautotrophy pathways. Metagenomic and metatranscriptomic fragment recruitment will be used to determine global patterns of chemoautotroph distribution and chemoautotrophy pathway expression. This ambitious project is made possible by the recent development of techniques and facilities for high-throughput genomic DNA recovery from individual cells at Bigelow Laboratory, genomic sequencing support provided by the U.S. Department of Energy Joint Genome Institute, and the establishment of a broad network of collaborations among many leading dark ocean microbiologists. Broader Impacts. One beginning researcher will be involved in this project as a co-PI, providing first-hand exposure to grant writing, project management and undergraduate student mentorship. The project will generate a large quantity of unique reference materials, laying a solid foundation for future studies of dark ocean microorganisms, including 207 microbial genomes, representing all major taxonomic groups of bacteria and archaea from the dark ocean, multiple metagenomes, metatranscriptomes and pyrotag data sets, as well as genomic DNA from ~2,000 individual cells from diverse prokaryote taxonomic groups, water masses and geographic locations. The work will improve our understanding of the global carbon cycle, with direct relevance to climate change studies. Further improvements in single cell genomics technology and its accessibility will likely benefit human health-related studies (e.g. human microbiome and cancer research) and bioprospecting for new energy sources and natural products.

Publications Produced as a Result of this Research

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Luo H, Swan BK, Stepanauskas R, Hughes AL, Moran MA "Evolutionary analysis of a streamlined lineage of surface ocean Roseobacters" The ISME Journal, v.8, 2014, p.1428.

Thrash, J Cameron and Temperton, Ben and Swan, Brandon K and Landry, Zachary C and Woyke, Tanja and DeLong, Edward F and Stepanauskas, Ramunas and Giovannoni, Stephan J "{Single-cell enabled comparative genomics of a deep ocean SAR11 bathytype.}" The ISME journal, v.8, 2014, p.1440--51. doi:10.1038/ismej.2013.243 

Lloyd, Karen G and Schreiber, Lars and Petersen, Dorthe G and Kjeldsen, Kasper U and Lever, Mark A and Steen, Andrew D and Stepanauskas, Ramunas and Richter, Michael and Kleindienst, Sara and Lenk, Sabine and Schramm, Andreas and J{\o}rgensen, Bo Barker "{Predominant archaea in marine sediments degrade detrital proteins}" Nature, v.496, 2013, p.215--218. doi:10.1038/nature12033 

Wasmund, Kenneth and Cooper, Myriel and Schreiber, Lars and Lloyd, Karen G. and Baker, Brett J. and Petersen, Dorthe G. and Joergensen, Bo Barker and Stepanauskas, Ramunas and Reinhardt, Richard and Schramm, Andreas and Loy, Alexander and Adrian, Lorenz "{Single-cell genome and group-specific dsrAB sequencing implicate marine members of the class Dehalococcoidia (phylum Chloroflexi) in sulfur cycling}" mBio, v.7, 2016, p.. doi:10.1128/mBio.00266-16 

Kminek G, Conley C, Allen CC, Bartlett DH, Beaty DW, Benning LG, Bhartia R, Boston PJ, Duchaine C, Farmer JD, Flynn GJ, Glavin DP, Gorby Y, Hallsworth JE, Mogul R, Moser D, Buford Price P, Pukall R, Fernandez-Remolar D, Smith CL, Stedman K, Steele A, Step "Report of the workshop for life detection in samples from Mars" Life Sciences in Space Research, v.2, 2014, p.1.

Rinke C, Schwientek P, Sczyrba A, Ivanova NN, Anderson IJ, Cheng JF, Darling A, Malfatti S, Swan BK, Gies EA, Dodsworth JA, Hedlund BP, Tsiamis G, Sievert SM, Liu WT, Eisen JA, Hallam S, Kyrpides N, Stepanauskas R, Rubin E, Hugenholtz P, Woyke T "Insights into the phylogeny and coding potential of microbial dark matter." Nature, v.499, 2013, p.431. doi:10.1038/nature12352 

Wasmund, Kenneth and Schreiber, Lars and Lloyd, Karen G and Petersen, Dorthe G and Schramm, Andreas and Stepanauskas, Ramunas and Joergensen, Bo Barker and Adrian, Lorenz "{Genome sequencing of a single cell of the widely distributed marine subsurface Dehalococcoidia, phylum Chloroflexi.}" The ISME journal, v.8, 2014, p.383--97. doi:10.1038/ismej.2013.143 

Zhang, Yao and Sun, Ying and Jiao, Nianzhi and Stepanauskas, Ramunas and Luo, Haiwei "Ecological genomics of the uncultivated marine Roseobacter lineage CHAB-I-5" Applied and Environmental Microbiology, v.82, 2016, p.2100--211. doi:10.1128/AEM.03678-15 

Martijn J, Schullz F, Zaremba-Niedzwiedzka K, Viklund J, Stepanauskas R, Andersson SGE, Horn M, Guy L, Ettema TJG. "Single cell genomics of a rare environmental alphaproteobacterium provides unique insights into Rickettsiaceae evolution." The ISME Journal, v., 2015, p..

Stepanauskas Ramunas "Wiretapping into microbial interactions by single cell genomics" Frontiers in Microbiology, v.6, 2015, p.. doi:10.3389/fmicb.2015.00258 

Luo, Haiwei and Swan, Brandon K and Stepanauskas, Ramunas and Hughes, Austin L and Moran, Mary Ann "{Evolutionary analysis of a streamlined lineage of surface ocean Roseobacters.}" The ISME journal, v.8, 2014, p.1428--39. doi:10.1038/ismej.2013.248 

Kashtan, Nadav and Roggensack, Sara E and Rodrigue, S{\'{e}}bastien and Thompson, Jessie W and Biller, Steven J and Coe, Allison and Ding, Huiming and Marttinen, Pekka and Malmstrom, Rex R and Stocker, Roman and Follows, Michael J and Stepanauskas, Ramuna "{Single-cell genomics reveals hundreds of coexisting subpopulations in wild Prochlorococcus.}" Science (New York, N.Y.), v.344, 2014, p.416--20. doi:10.1126/science.1248575 

Rinke C, Lee J, Nath N, Goudeau D, Thompson B, Poulton N, Ferguson E, Malmstrom R, Stepanauskas R, Woyke T. "Obtaining genomes from uncultivated environmental microorganisms." Nature Protocols, v.9, 2014, p.1038.

Luo, Haiwei and Swan, Brandon K. and Stepanauskas, Ramunas and Hughes, Austin L. and Moran, Mary Ann "{Comparing effective population sizes of dominant marine alphaproteobacteria lineages}" Environmental Microbiology Reports, v.6, 2014, p.167--172. doi:10.1111/1758-2229.12129 

Ghylin TW, Garcia SL, Moya F, Oyserman BO, Schwientek P, Forest KT, Mutschler J, Dwulit-Smith J, Chan LK, Martinez-Garcia M, Sczyrba A, Stepanauskas R, Grossart HP, Woyke T, Warnecke F, Malmstrom R, Bertilsson S, McMahon KD. "Comparative single-cell genomics reveals potential ecological niches for the freshwater acI Actinobacteria lineage." The ISME Journal, v.8, 2014, p.2503.

Eiler, Alexander and Zaremba-Niedzwiedzka, Katarzyna and Martinez-Garcia, Manuel and Mcmahon, Katherine D. and Stepanauskas, Ramunas and Andersson, Siv G E and Bertilsson, Stefan "{Productivity and salinity structuring of the microplankton revealed by comparative freshwater metagenomics}" Environmental Microbiology, v.16, 2014, p.2682--269. doi:10.1111/1462-2920.12301 

Roux S, Hawley AK, Beltran MT, Scofield M, Schwientek P, Stepanauskas R, Woyke T, Hallam SJ, Sullivan MB. "Ecology and evolution of viruses infecting uncultivated SUP05 bacteria as revealed by single-cell- and meta-genomics." eLife, v.3, 2014, p.03125.

Kminek, Gerhard and Conley, Catherine and Allen, Carlton C. and Bartlett, Douglas H. and Beaty, David W. and Benning, Liane G. and Bhartia, Rohit and Boston, Penelope J. and Duchaine, Caroline and Farmer, Jack D. and Flynn, George J. and Glavin, Daniel P. "{Report of the workshop for life detection in samples from Mars}" Life Sciences in Space Research, v.2, 2014, p.1--5. doi:10.1016/j.lssr.2014.05.001 

Luo, Haiwei and Tolar, Bradley B and Swan, Brandon K and Zhang, Chuanlun L and Stepanauskas, Ramunas and {Ann Moran}, Mary and Hollibaugh, James T "{Single-cell genomics shedding light on marine Thaumarchaeota diversification.}" The ISME journal, v.8, 2014, p.732--6. doi:10.1038/ismej.2013.202 

Swan, BK, M Chaffin, M Martinez-Garcia, HG Morrison, E Field, NJ Poulton, EDP Masland, CC Harris, A Sczyrba, PSG Chain, S Koren, T Woyke and R Stepanauskas "Genomic and metabolic diversity of Marine Group I Thaumarchaeota in the mesopelagic of two subtropical gyres" PLoS ONE, v.9, 2014, p.e95380. doi:10.1371/journal.pone.0095380 

Swan BK, Tupper B, Sczyrba A, Lauro FM, Martinez-Garcia M, González JM, Luo H, Wright JJ, Landry ZC, Hanson NW, Thompson BP, Poulton NJ, Schwientek P, Acinas SG, Giovannoni SJ, Moran MA, Hallam SJ, Cavicchioli R, Woyke T, Stepanauskas, R "Prevalent genome streamlining and latitudinal divergence of marine planktonic bacteria in the surface ocean" PNAS, v.TBD, 2013, p.TBD. doi:10.1073/pnas.1304246110 

Labonte JM, Field EK, Lau M, Chivian D, van Heerden E, Wommack KE, Kieft TL, Onstott TC, Stepanauskas R. "Single cell genomics indicates horizontal gene transfer and viral infections in a deep subsurface Firmicutes population" Frontiers in Microbiology, v.6, 2015, p.649.

Luo, Haiwei and Tolar, Bradley B and Swan, Brandon K and Zhang, Chuanlun L and Stepanauskas, Ramunas and Ann Moran, Mary and Hollibaugh, James T "Single-cell genomics shedding light on marine Thaumarchaeota diversification" {ISME} J, v.8, 2014, p.732--736. doi:1751-7362 

Martijn, Joran and Schulz, Frederik and Zaremba-Niedzwiedzka, Katarzyna and Viklund, Johan and Stepanauskas, Ramunas and Andersson, Siv G E and Horn, Matthias and Guy, Lionel and Ettema, Thijs J G "{Single-cell genomics of a rare environmental alphaproteobacterium provides unique insights into Rickettsiaceae evolution.}" The ISME journal, v.9, 2015, p.2373--85. doi:10.1038/ismej.2015.46 

Stepanauskas R "Wiretapping into microbial interactions by single cell genomics" Frontiers in Microbiology, v.6, 2015, p.258.

Labonté JM, Swan BK, Poulos B, Luo H, Koren S, Hallam SJ, Sullivan MB, Woyke T, Wommack KE, Stepanauskas R. "Single cell genomics-based analysis of virus-host interactions in marine surface bacterioplankton." The ISME Journal, v., 2015, p..

Ngugi, D.K. and Blom, J. and Stepanauskas, R. and Stingl, U. "{Diversification and niche adaptations of Nitrospina-like bacteria in the polyextreme interfaces of Red Sea brines}" The ISME Journal, v., 2015, p.1--17. doi:10.1038/ismej.2015.214 

Swan, Brandon K. and Tupper, Ben and Sczyrba, Alexander and Lauro, Federico M. and Martinez-Garcia, Manuel and González, José M. and Luo, Haiwei and Wright, Jody J. and Landry, Zachary C. and Hanson, Niels W. and Thompson, Brian P. and Poulton, Nicole J. "Prevalent genome streamlining and latitudinal divergence of planktonic bacteria in the surface ocean" Proceedings of the National Academy of Sciences, v., 2013, p.. doi:10.1073/pnas.1304246110 

Stepanauskas R. "Crystal Ball: Re-defining microbial diversity from its single-celled building blocks." Environmental Microbiology Reports, v.7, 2015, p.36.

Labont{\'{e}}, Jessica M and Swan, Brandon K and Poulos, Bonnie and Luo, Haiwei and Koren, Sergey and Hallam, Steven J and Sullivan, Matthew B and Woyke, Tanja and {Eric Wommack}, K and Stepanauskas, Ramunas "{Single-cell genomics-based analysis of virus?host interactions in marine surface bacterioplankton}" The ISME Journal, v.9, 2015, p.2386--239. doi:10.1038/ismej.2015.48 

Rinke, Christian and Lee, Janey and Nath, Nandita and Goudeau, Danielle and Thompson, Brian and Poulton, Nicole and Dmitrieff, Elizabeth and Malmstrom, Rex and Stepanauskas, Ramunas and Woyke, Tanja "{Obtaining genomes from uncultivated environmental microorganisms using FACS?based single-cell genomics}" Nat. Protocols, v.9, 2014, p.1038--104. doi:1754-2189 

Wasmund K, Schreiber L, Lloyd KG, Petersen DG, Schramm A, Stepanauskas R, Jørgensen BB, Adrian L. "Genome sequencing of a single cell of the widely distributed marine subsurface Dehalococcoidia, phylum Chloroflexi." The ISME Journal, v.8, 2014, p.383.

Ghylin, T W and Garcia, S L and Moya, F and Oyserman, B O and Schwientek, P and Forest, K T and Mutschler, J and Dwulit-Smith, J and Chan, L K and Martinez-Garcia, M and Sczyrba, A and Stepanauskas, R and Grossart, H P and Woyke, T and Warnecke, F and Mal "{Comparative single-cell genomics reveals potential ecological niches for the freshwater acI Actinobacteria lineage}" Isme j, v.8, 2014, p.2503--251. doi:10.1038/ismej.2014.135 

Rinke, Christian and Schwientek, Patrick and Sczyrba, Alexander and Ivanova, Natalia N and Anderson, Iain J and Cheng, Jan-Fang and Darling, Aaron E and Malfatti, Stephanie and Swan, Brandon K and Gies, Esther a and Dodsworth, Jeremy a and Hedlund, Brian "{Insights into the phylogeny and coding potential of microbial dark matter.}" Nature, v.499, 2013, p.431--437. doi:10.1038/nature12352 

Labont{\'{e}}, Jessica M. and Field, Erin K. and Lau, Maggie and Chivian, Dylan and {Van Heerden}, Esta and Wommack, K. Eric and Kieft, Thomas L. and Onstott, Tullis C. and Stepanauskas, Ramunas "{Single cell genomics indicates horizontal gene transfer and viral infections in a deep subsurface Firmicutes population}" Frontiers in Microbiology, v.6, 2015, p.. doi:10.3389/fmicb.2015.00349 

Roux, Simon and Hawley, Alyse K. and Beltran, Monica Torres and Scofeld, Melanie and Schwientek, Patrick and Stepanauskas, Ramunas and Woyke, Tanja and Hallam, Steven J. and Sullivan, Matthew B. "{Ecology and evolution of viruses infecting uncultivated SUP05 bacteria as revealed by single-cell- and meta-genomics}" eLife, v.2014, 2014, p.. doi:10.7554/eLife.03125.001 

Dyksma, Stefan and Bischof, Kerstin and Fuchs, Bernhard M and Hoffmann, Katy and Meier, Dimitri and Meyerdierks, Anke and Pjevac, Petra and Probandt, David and Richter, Michael and Stepanauskas, Ramunas and Mu{\ss}mann, Marc "{Ubiquitous Gammaproteobacteria dominate dark carbon fixation in coastal sediments}" The ISME journal, v., 2016, p.1--15. doi:10.1038/ISMEJ.2015.257 

Kashtan N, Roggensack SE, Rodrigue S, Thompson JW, Biller SJ, Coe A, Ding H, Marttinen P, Malmstrom R, Stocker R, Follows MJ, Stepanauskas R, Chisholm SW "Single cell genomics reveals hundreds of coexisting subpopulations in wild Prochlorococcus" Science, v.344, 2014, p.416.

Luo H, Swan BK, Stepanauskas R, Hughes AL, Moran MA "Comparing Effective Population Sizes of Dominant Marine Alphaproteobacteria Lineages." Environmental Microbiology Reports, v.6, 2014, p.167.

Stepanauskas, Ramunas "Re-defining microbial diversity from its single-celled building blocks" Environmental Microbiology Reports, v.7, 2015, p.36--37. doi:10.1111/1758-2229.12226 

Swan, Brandon K and Tupper, Ben and Sczyrba, Alexander and Lauro, Federico M and Martinez-Garcia, Manuel and Gonzalez, Jose M and Luo, Haiwei and Wright, Jody J and Landry, Zachary C and Hanson, Niels W and Thompson, Brian P and Poulton, Nicole J and Schw "{Prevalent genome streamlining and latitudinal divergence of planktonic bacteria in the surface ocean.}" Proceedings of the National Academy of Sciences of the United States of America, v.110, 2013, p.11463--8. doi:10.1073/pnas.1304246110 

Swan, Brandon K. and Chaffin, Mark D. and Martinez-Garcia, Manuel and Morrison, Hilary G. and Field, Erin K. and Poulton, Nicole J. and Masland, E. Dashiell P and Harris, Christopher C. and Sczyrba, Alexander and Chain, Patrick S G and Koren, Sergey and W "{Genomic and metabolic diversity of marine group i thaumarchaeota in the mesopelagic of two subtropical gyres}" PLoS ONE, v.9, 2014, p.. doi:10.1371/journal.pone.0095380 

Cameron Thrash, J and Temperton, Ben and Swan, Brandon K and Landry, Zachary C and Woyke, Tanja and DeLong, Edward F and Stepanauskas, Ramunas and Giovannoni, Stephan J "Single-cell enabled comparative genomics of a deep ocean {SAR11} bathytype" {ISME} J, v., 2014, p.. doi:1751-7370 

Eiler A, Zaremba-Niedzwiedzka K, Martinez-Garcia M, McMahon KD, Stepanauskas R, Andersson SGE, Bertilsson S. "Productivity and salinity structuring of the microplankton revealed by comparative freshwater metagenomics." Environmental Microbiology, v.16, 2014, p.2682.


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.

Overview. Over 90% of ocean's volume is too deep for the sunlight to penetrate and support photosynthesis. The dark realm of the ocean is one of the largest environments inhabited by life on our planet. Dark ocean's microorganisms play a major role in the global cycling of carbon and other elements, both by remineralizing the organic compounds produced at ocean's surface and by synthesizing new biomass from inorganic constituents through chemoautotrophy. The specific biochemical reactions, energy sources and microbial groups involved in the chemoautotrophic carbon fixation in the dark ocean remained poorly understood, to a large degree due to difficulties in laboratory cultivation of relevant representatives. This project aimed at addressing some of the key knowledge gaps about the chemoautotrophy in the dark ocean, primarily by utilizing single cell genomics and other cutting-edge, cultivation-independent research tools.

Intellectual merit. During the course of this project, we analyzed dark ocean samples from locations around the globe and down to the greatest depths, including the Challenger Deep at the bottom of the Marianna Trench. A large group of collaborating scientists were engaged in the analysis of the genetic information encoded in over 3,000 individual cells of microorganisms from these samples. This resulted in a major advance in our understanding of the taxonomic composition, geographic distribution, genomic content and metabolic potential of chemoautotrophs in the dark ocean, with a synergistic impact on other fields of microbial oceanography. Examples of research findings include: a) identification of chemoautotrophy pathways in diverse groups of archaea and bacteria; b) confirmation of ammonium and reduced sulfur oxidation as common sources of energy for chemoautotrophs in oxygenated dark ocean; c) estimates of the contribution of nitrite oxidizing bacteria to the marine dark carbon fixation; d) indications of the importance of extensive metabolic interdependencies among chemoautotrophs; e) improved models for the early evolution of bacteria and archaea; f) systematic differences between cultured and uncultured marine microorganisms; and g) strong latitudinal and vertical divergence of marine bacterioplankton composition. Project's findings were reported in 24 peer-reviewed publications (of them, four in Science, Nature and PNAS), 49 presentations, and 14 additional manuscripts that are in review or in preparation. Project's data can be accessed here: http://www.bco-dmo.org/project/471826.

Broader impacts. This project supported training of four postdoctoral researchers and eight other professionals (computational and laboratory scientists) who were involved in various aspects of laboratory work, computational analyses, result presentations and manuscript preparation, thus obtaining hands-on experience in new research areas and technologies, as well as project management and mentorship skills. Two undergraduate students were engaged in this project in the framework of the Bigelow Research Experiences for Undergraduates (REU) program, a nationally ranked and competitive program that provides research experience in oceanography for college undergraduates across the United States. Both students excelled in their work, incorporated project results in their theses and presented findings at international science conferences. More than 50 additional students and postdoctoral scientists at collaborating institutions also received training from this project. Improvements in the single cell genomics technology, in part supported by this project, were incorporated into Bigelow Laboratory Single Cell Genomics Center's services. The SCGC serves a wide range of research projects in over 100 organizations around the globe. The ultimate goals of these projects range from basic science to applications such as environmental monitoring (e.g. oil spills) and technology (e.g. wastewater treatment plants), energy production and bioprospecting (e.g. mining industry), human health (e.g. cancer, microbiome), and law enforcement and national security (forensics).


Last Modified: 12/04/2016
Modified by: Ramunas Stepanauskas

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