Single-colony MALDI mass spectrometry imaging reveals spatial differences in metabolite abundance between natural and cultured Trichodesmium morphotypes

Romanowicz, Karl J.; Zhang, Futing; Wang, Siyuan; Veličković, Dušan; Chu, Rosalie K.; Shaked, Yeala; Boiteau, Rene M.

doi:10.1128/msystems.01152-24

Title: Single-colony MALDI mass spectrometry imaging reveals spatial differences in metabolite abundance between natural and cultured Trichodesmium morphotypes

Journal Article · 23 September 2024 · mSystems

DOI: https://doi.org/10.1128/msystems.01152-24 · OSTI ID:2474715

^[1]; Zhang, Futing ^[2]; Wang, Siyuan ^[2];

^[3]; Chu, Rosalie K. ^[3]; Shaked, Yeala ^[2];

^[4]

Oregon State Univ., Corvallis, OR (United States)
Hebrew Univ. of Jerusalem (Israel); The Interuniversity Institute for Marine Sciences, Eilat (Israel)
Pacific Northwest National Laboratory (PNNL), Richland, WA (United States)
Oregon State Univ., Corvallis, OR (United States); Univ. of Minnesota, Minneapolis, MN (United States)

Trichodesmium, a globally significant N₂-fixing marine cyanobacterium, forms extensive surface blooms in nutrient-poor ocean regions. These blooms consist of a dynamic assemblage of Trichodesmium species that form distinct colony morphotypes and are inhabited by diverse microorganisms. Trichodesmium colony morphotypes vary in ecological niche, nutrient uptake, and organic molecule release, differentially impacting ocean carbon and nitrogen biogeochemical cycles. Here, we assessed the poorly studied spatial abundance of metabolites within and between three morphologically distinct Trichodesmium colonies collected from the Red Sea. We also compared these results with two morphotypes of the cultivable Trichodesmium strain IMS101. Using matrix-assisted laser desorption/ionization (MALDI) mass spectrometry imaging (MSI) coupled with liquid extraction surface analysis (LESA) tandem mass spectrometry (MS2), we identified and localized a wide range of small metabolites associated with single-colony Trichodesmium morphotypes. Our untargeted MALDI-MSI approach revealed 80 unique features (metabolites) shared between Trichodesmium morphotypes. Discrimination analysis showed spatial variations in 57 shared metabolites, accounting for 62% of the observed variation between morphotypes. The greatest variations in metabolite abundance were observed between the cultured morphotypes compared to the natural colony morphotypes, suggesting substantial differences in metabolite production between the cultivable strain IMS101 and the naturally occurring colony morphotypes that the cultivable strain is meant to represent. This study highlights the variations in metabolite abundance between natural and cultured Trichodesmium morphotypes and provides valuable insights into metabolites common to morphologically distinct Trichodesmium colonies, offering a foundation for future targeted metabolomic investigations.

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Research Organization:: Pacific Northwest National Laboratory (PNNL), Richland, WA (United States)

Sponsoring Organization:: Simons Foundation; USDOE Office of Science (SC), Basic Energy Sciences (BES). Scientific User Facilities (SUF); USDOE Office of Science (SC), Biological and Environmental Research (BER); United States-Israel Binational Science Foundation (BSF)

Grant/Contract Number:: AC02-05CH11231; AC05-76RL01830

OSTI ID:: 2474715

Report Number(s):: PNNL-SA--204009

Journal Information:: mSystems, Journal Name: mSystems Journal Issue: 10 Vol. 9; ISSN 2379-5077

Publisher:: American Society for MicrobiologyCopyright Statement

Country of Publication:: United States

Language:: English

References (57)

Mineral iron utilization by natural and cultured Trichodesmium and associated bacteria: Mineral Fe utilization by Trichodesmium and bacteria Basu, Subhajit; Shaked, Yeala Limnology and Oceanography, Vol. 63, Issue 6 https://doi.org/10.1002/lno.10939	journal	July 2018
The Trichodesmium microbiome can modulate host N₂ fixation Frischkorn, Kyle R.; Rouco, Mónica; Van Mooy, Benjamin A. S. Limnology and Oceanography Letters, Vol. 3, Issue 6 https://doi.org/10.1002/lol2.10092	journal	October 2018
Liquid extraction surface analysis mass spectrometry (LESA-MS) as a novel profiling tool for drug distribution and metabolism analysis: the terfenadine example: LESA-MS distribution analysis of terfenadine Eikel, Daniel; Vavrek, Marissa; Smith, Sheri Rapid Communications in Mass Spectrometry, Vol. 25, Issue 23 https://doi.org/10.1002/rcm.5274	journal	November 2011
Laboratory culture studies of Trichodesmium isolated from the Great Barrier Reef Lagoon, Australia Bell, Peter R. F.; Uwins, Philippa J. R.; Elmetri, Ibrahim Hydrobiologia, Vol. 532, Issue 1-3 https://doi.org/10.1007/s10750-004-8768-1	journal	January 2005
High-resolution AP-SMALDI mass spectrometry imaging of Drosophila melanogaster Khalil, S. M.; Pretzel, J.; Becker, K. International Journal of Mass Spectrometry, Vol. 416 https://doi.org/10.1016/j.ijms.2017.04.001	journal	May 2017
Colonies of the marine cyanobacterium Trichodesmium optimize dust utilization by selective collection and retention of nutrient-rich particles Wang, Siyuan; Koedooder, Coco; Zhang, Futing iScience, Vol. 25, Issue 1 https://doi.org/10.1016/j.isci.2021.103587	journal	January 2022
Better together? Lessons on sociality from Trichodesmium Eichner, Meri; Inomura, Keisuke; Pierella Karlusich, Juan José Trends in Microbiology, Vol. 31, Issue 10 https://doi.org/10.1016/j.tim.2023.05.001	journal	October 2023
Multimodal MSI in Conjunction with Broad Coverage Spatially Resolved MS ² Increases Confidence in Both Molecular Identification and Localization Veličković, Dušan; Chu, Rosalie K.; Carrell, Alyssa A. Analytical Chemistry, Vol. 90, Issue 1 https://doi.org/10.1021/acs.analchem.7b04319	journal	December 2017
The Natural Products Atlas: An Open Access Knowledge Base for Microbial Natural Products Discovery van Santen, Jeffrey A.; Jacob, Grégoire; Singh, Amrit Leen ACS Central Science, Vol. 5, Issue 11 https://doi.org/10.1021/acscentsci.9b00806	journal	September 2019
Nitrogen fixation by Trichodesmium spp.: An important source of new nitrogen to the tropical and subtropical North Atlantic Ocean Capone, Douglas G.; Burns, James A.; Montoya, Joseph P. Global Biogeochemical Cycles, Vol. 19, Issue 2 https://doi.org/10.1029/2004GB002331	journal	June 2005
Global patterns of marine nitrogen fixation and denitrification Gruber, Nicolas; Sarmiento, Jorge L. Global Biogeochemical Cycles, Vol. 11, Issue 2 https://doi.org/10.1029/97GB00077	journal	June 1997
Quorum sensing in Cyanobacteria: N-octanoyl-homoserine lactone release and response, by the epilithic colonial cyanobacterium Gloeothece PCC6909 Sharif, Dilara I.; Gallon, John; Smith, Chris J. The ISME Journal, Vol. 2, Issue 12 https://doi.org/10.1038/ismej.2008.68	journal	July 2008
Microbial community gene expression within colonies of the diazotroph, Trichodesmium, from the Southwest Pacific Ocean Hewson, Ian; Poretsky, Rachel S.; Dyhrman, Sonya T. The ISME Journal, Vol. 3, Issue 11 https://doi.org/10.1038/ismej.2009.75	journal	July 2009
Quorum sensing control of phosphorus acquisition in Trichodesmium consortia Van Mooy, Benjamin A. S.; Hmelo, Laura R.; Sofen, Laura E. The ISME Journal, Vol. 6, Issue 2 https://doi.org/10.1038/ismej.2011.115	journal	September 2011
Chemical microenvironments and single-cell carbon and nitrogen uptake in field-collected colonies of Trichodesmium under different pCO2 Eichner, Meri J.; Klawonn, Isabell; Wilson, Samuel T. The ISME Journal, Vol. 11, Issue 6 https://doi.org/10.1038/ismej.2017.15	journal	April 2017
The Trichodesmium consortium: conserved heterotrophic co-occurrence and genomic signatures of potential interactions Lee, Michael D.; Walworth, Nathan G.; McParland, Erin L. The ISME Journal, Vol. 11, Issue 8 https://doi.org/10.1038/ismej.2017.49	journal	April 2017
Epibionts dominate metabolic functional potential of Trichodesmium colonies from the oligotrophic ocean Frischkorn, Kyle R.; Rouco, Mónica; Van Mooy, Benjamin A. S. The ISME Journal, Vol. 11, Issue 9 https://doi.org/10.1038/ismej.2017.74	journal	May 2017
Dust- and mineral-iron utilization by the marine dinitrogen-fixer Trichodesmium Rubin, Maxim; Berman-Frank, Ilana; Shaked, Yeala Nature Geoscience, Vol. 4, Issue 8 https://doi.org/10.1038/ngeo1181	journal	June 2011
FDR-controlled metabolite annotation for high-resolution imaging mass spectrometry Palmer, Andrew; Phapale, Prasad; Chernyavsky, Ilya Nature Methods, Vol. 14, Issue 1 https://doi.org/10.1038/nmeth.4072	journal	November 2016
Benefit from decline: the primary transcriptome of Alteromonas macleodii str. Te101 during Trichodesmium demise Hou, Shengwei; López-Pérez, Mario; Pfreundt, Ulrike The ISME Journal, Vol. 12, Issue 4 https://doi.org/10.1038/s41396-017-0034-4	journal	January 2018
Iron and phosphorus deprivation induce sociality in the marine bloom-forming cyanobacterium Trichodesmium Tzubari, Yael; Magnezi, Liel; Be’er, Avraham The ISME Journal, Vol. 12, Issue 7 https://doi.org/10.1038/s41396-018-0073-5	journal	February 2018
Selective collection of iron-rich dust particles by natural Trichodesmium colonies Kessler, Nivi; Armoza-Zvuloni, Rachel; Wang, Siyuan The ISME Journal, Vol. 14, Issue 1 https://doi.org/10.1038/s41396-019-0505-x	journal	September 2019
Distinct nitrogen cycling and steep chemical gradients in Trichodesmium colonies Klawonn, Isabell; Eichner, Meri J.; Wilson, Samuel T. The ISME Journal, Vol. 14, Issue 2 https://doi.org/10.1038/s41396-019-0514-9	journal	October 2019
Structural bases for aspartate recognition and polymerization efficiency of cyanobacterial cyanophycin synthetase Miyakawa, Takuya; Yang, Jian; Kawasaki, Masato Nature Communications, Vol. 13, Issue 1 https://doi.org/10.1038/s41467-022-32834-8	journal	August 2022
Ultra-High Mass Resolution MALDI Imaging Mass Spectrometry of Proteins and Metabolites in a Mouse Model of Glioblastoma Dilillo, M.; Ait-Belkacem, R.; Esteve, C. Scientific Reports, Vol. 7, Issue 1 https://doi.org/10.1038/s41598-017-00703-w	journal	April 2017
Imaging mass spectrometry and MS/MS molecular networking reveals chemical interactions among cuticular bacteria and pathogenic fungi associated with fungus-growing ants Boya P., Cristopher A.; Fernández-Marín, Hermógenes; Mejía, Luis C. Scientific Reports, Vol. 7, Issue 1 https://doi.org/10.1038/s41598-017-05515-6	journal	July 2017
Colonies of marine cyanobacteria Trichodesmium interact with associated bacteria to acquire iron from dust Basu, Subhajit; Gledhill, Martha; de Beer, Dirk Communications Biology, Vol. 2, Issue 1 https://doi.org/10.1038/s42003-019-0534-z	journal	August 2019
Mechanisms and heterogeneity of in situ mineral processing by the marine nitrogen fixer Trichodesmium revealed by single-colony metaproteomics Held, Noelle A.; Sutherland, Kevin M.; Webb, Eric A. ISME Communications, Vol. 1, Issue 1 https://doi.org/10.1038/s43705-021-00034-y	journal	July 2021
Importance of mobile genetic element immunity in numerically abundant Trichodesmium clades Webb, Eric A.; Held, Noelle A.; Zhao, Yiming ISME Communications, Vol. 3, Issue 1 https://doi.org/10.1038/s43705-023-00214-y	journal	February 2023
Towards resolving the spatial metabolome with unambiguous molecular annotations in complex biological systems by coupling mass spectrometry imaging with structures for lossless ion manipulations Nagy, Gabe; Veličković, Dusan; Chu, Rosalie K. Chemical Communications, Vol. 55, Issue 3 https://doi.org/10.1039/c8cc07482h	journal	January 2019
Metallophores associated with Trichodesmium erythraeum colonies from the Gulf of Aqaba Gledhill, Martha; Basu, Subhajit; Shaked, Yeala Metallomics, Vol. 11, Issue 9 https://doi.org/10.1039/c9mt00121b	journal	January 2019
Fixation and fate of C and N in the cyanobacterium Trichodesmium using nanometer-scale secondary ion mass spectrometry Finzi-Hart, J. A.; Pett-Ridge, J.; Weber, P. K. Proceedings of the National Academy of Sciences, Vol. 106, Issue 15 https://doi.org/10.1073/pnas.0810547106	journal	March 2009
Trimethylated homoserine functions as the major compatible solute in the globally significant oceanic cyanobacterium Trichodesmium Pade, Nadin; Michalik, Dirk; Ruth, Wolfgang Proceedings of the National Academy of Sciences, Vol. 113, Issue 46 https://doi.org/10.1073/pnas.1611666113	journal	October 2016
Receiver Operating Characteristic Methodology Pepe, Margaret Sullivan Journal of the American Statistical Association, Vol. 95, Issue 449 https://doi.org/10.1080/01621459.2000.10473930	journal	March 2000
ChEBI in 2016: Improved services and an expanding collection of metabolites Hastings, Janna; Owen, Gareth; Dekker, Adriano Nucleic Acids Research, Vol. 44, Issue D1 https://doi.org/10.1093/nar/gkv1031	journal	October 2015
KEGG: new perspectives on genomes, pathways, diseases and drugs Kanehisa, Minoru; Furumichi, Miho; Tanabe, Mao Nucleic Acids Research, Vol. 45, Issue D1 https://doi.org/10.1093/nar/gkw1092	journal	November 2016
HMDB 4.0: the human metabolome database for 2018 Wishart, David S.; Feunang, Yannick Djoumbou; Marcu, Ana Nucleic Acids Research, Vol. 46, Issue D1 https://doi.org/10.1093/nar/gkx1089	journal	November 2017
The microbial and metazoan community associated with colonies of Trichodesmium spp.: a quantitative survey Sheridan, C. C. Journal of Plankton Research, Vol. 24, Issue 9 https://doi.org/10.1093/plankt/24.9.913	journal	September 2002
Modulation of violacein production and phenotypes associated with biofilm by exogenous quorum sensing N-acylhomoserine lactones in the marine bacterium Pseudoalteromonas ulvae TC14 Mireille Ayé, Armande; Bonnin-Jusserand, Maryse; Brian-Jaisson, Florence Microbiology, Vol. 161, Issue 10 https://doi.org/10.1099/mic.0.000147	journal	October 2015
Microbial diversity within the T richodesmium holobiont Rouco, Mónica; Haley, Sheean T.; Dyhrman, Sonya T. Environmental Microbiology, Vol. 18, Issue 12 https://doi.org/10.1111/1462-2920.13513	journal	September 2016
Effects of iron limitation on the expression of metabolic genes in the marine cyanobacterium Trichodesmium erythraeum IMS101 Shi, Tuo; Sun, Yi; Falkowski, Paul G. Environmental Microbiology, Vol. 9, Issue 12 https://doi.org/10.1111/j.1462-2920.2007.01406.x	journal	December 2007
Regulation of nitrogen metabolism in the marine diazotroph Trichodesmium IMS101 under varying temperatures and atmospheric CO2 concentrations: CO2, temperature and Trichodesmium's nitrogen metabolism Levitan, Orly; Brown, Christopher M.; Sudhaus, Stefanie Environmental Microbiology, Vol. 12, Issue 7 https://doi.org/10.1111/j.1462-2920.2010.02195.x	journal	March 2010
Comparison of Cultured Trichodesmium (Cyanophyceae) with Species Characterized from the Field1: Trichodesmium Characterization Hynes, Annette M.; Webb, Eric A.; Doney, Scott C. Journal of Phycology, Vol. 48, Issue 1 https://doi.org/10.1111/j.1529-8817.2011.01096.x	journal	December 2011
Combined effects of different CO ₂ levels and N sources on the diazotrophic cyanobacterium Trichodesmium Eichner, Meri; Kranz, Sven A.; Rost, Björn Physiologia Plantarum, Vol. 152, Issue 2 https://doi.org/10.1111/ppl.12172	journal	March 2014
Trichodesmium, a Globally Significant Marine Cyanobacterium Capone, D. G. Science, Vol. 276, Issue 5316 https://doi.org/10.1126/science.276.5316.1221	journal	May 1997
Transcriptional Activities of the Microbial Consortium Living with the Marine Nitrogen-Fixing Cyanobacterium Trichodesmium Reveal Potential Roles in Community-Level Nitrogen Cycling Lee, Michael D.; Webb, Eric A.; Walworth, Nathan G. Applied and Environmental Microbiology, Vol. 84, Issue 1 https://doi.org/10.1128/AEM.02026-17	journal	October 2017
Taxonomic distribution of metabolic functions in bacteria associated with Trichodesmium consortia Koedooder, Coco; Zhang, Futing; Wang, Siyuan mSystems, Vol. 8, Issue 6 https://doi.org/10.1128/msystems.00742-23	journal	December 2023
Single-colony MALDI mass spectrometry imaging reveals spatial differences in metabolite abundance between natural and cultured Trichodesmium morphotypes Romanowicz, Karl J.; Zhang, Futing; Wang, Siyuan mSystems, Vol. 9, Issue 10 https://doi.org/10.1128/msystems.01152-24	journal	October 2024
In silico fragmentation for computer assisted identification of metabolite mass spectra Wolf, Sebastian; Schmidt, Stephan; Müller-Hannemann, Matthias BMC Bioinformatics, Vol. 11, Issue 1 https://doi.org/10.1186/1471-2105-11-148	journal	March 2010
MetFrag relaunched: incorporating strategies beyond in silico fragmentation Ruttkies, Christoph; Schymanski, Emma L.; Wolf, Sebastian Journal of Cheminformatics, Vol. 8, Issue 1 https://doi.org/10.1186/s13321-016-0115-9	journal	January 2016
The conundrum of marine N2 fixation Mahaffey, C. American Journal of Science, Vol. 305, Issue 6-8 https://doi.org/10.2475/ajs.305.6-8.546	journal	June 2005
Nitrogen fixation, uptake and metabolism in natural and cultured populations of Trichodesmium spp. Mulholland, Mr; Capone, Dg Marine Ecology Progress Series, Vol. 188 https://doi.org/10.3354/meps188033	journal	January 1999
Detection of Diverse N-Acyl-Homoserine Lactones in Vibrio alginolyticus and Regulation of Biofilm Formation by N-(3-Oxodecanoyl) Homoserine Lactone In vitro Liu, Jianfei; Fu, Kaifei; Wang, Yuxiao Frontiers in Microbiology, Vol. 8 https://doi.org/10.3389/fmicb.2017.01097	journal	June 2017
Metagenomes of Red Sea Subpopulations Challenge the Use of Marker Genes and Morphology to Assess Trichodesmium Diversity Koedooder, Coco; Landou, Etai; Zhang, Futing Frontiers in Microbiology, Vol. 13 https://doi.org/10.3389/fmicb.2022.879970	journal	May 2022
Evidence of Quorum Sensing in Cyanobacteria by Homoserine Lactones: The Origin of Blooms Herrera, Natalia; Echeverri, Fernando Water, Vol. 13, Issue 13 https://doi.org/10.3390/w13131831	journal	June 2021
The demise of the marine cyanobacterium, Trichodesmium spp., via an autocatalyzed cell death pathway Berman-Frank, Ilana; Bidle, Kay D.; Haramaty, Liti Limnology and Oceanography, Vol. 49, Issue 4 https://doi.org/10.4319/lo.2004.49.4.0997	journal	July 2004
Assessment of relative phosphorus limitation of Trichodesmium spp. in the North Pacific, North Atlantic, and the north coast of Australia Sohm, Jill A.; Mahaffey, Claire; Capone, Douglas G. Limnology and Oceanography, Vol. 53, Issue 6 https://doi.org/10.4319/lo.2008.53.6.2495	journal	November 2008

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Related Subjects

59 BASIC BIOLOGICAL SCIENCES
Trichodesmium
colony morphotypes
liquid extraction surface analysis (LESA)
mass spectrometry imaging (MSI)
matrix-assisted laser desorption/ionization (MALDI)
metabolite abundance
untargeted metabolomics

Title: Single-colony MALDI mass spectrometry imaging reveals spatial differences in metabolite abundance between natural and cultured Trichodesmium morphotypes

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