Metabolite diversity among representatives of divergent Prochlorococcus ecotypes
ABSTRACT The euphotic zone of the surface ocean contains distinct physical-chemical regimes that vary in light and nutrient concentrations as an inverse function of depth. The most numerous phytoplankter of the mid- and low-latitude ocean is the picocyanobacterium Prochlorococcus, which consists of...
| Main Authors: | , , , , , , , , |
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| Format: | Article |
| Language: | English |
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American Society for Microbiology
2023-10-01
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| Series: | mSystems |
| Subjects: | |
| Online Access: | https://journals.asm.org/doi/10.1128/msystems.01261-22 |
| _version_ | 1797617631001313280 |
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| author | Elizabeth B. Kujawinski Rogier Braakman Krista Longnecker Jamie W. Becker Sallie W. Chisholm Keven Dooley Melissa C. Kido Soule Gretchen J. Swarr Kathryn Halloran |
| author_facet | Elizabeth B. Kujawinski Rogier Braakman Krista Longnecker Jamie W. Becker Sallie W. Chisholm Keven Dooley Melissa C. Kido Soule Gretchen J. Swarr Kathryn Halloran |
| author_sort | Elizabeth B. Kujawinski |
| collection | DOAJ |
| description | ABSTRACT The euphotic zone of the surface ocean contains distinct physical-chemical regimes that vary in light and nutrient concentrations as an inverse function of depth. The most numerous phytoplankter of the mid- and low-latitude ocean is the picocyanobacterium Prochlorococcus, which consists of ecologically distinct subpopulations (i.e., “ecotypes”). Ecotypes have different temperature, light, and nutrient optima and display distinct relative abundances along gradients of these niche dimensions. As a primary producer, Prochlorococcus fixes and releases organic carbon to neighboring microbes as part of the microbial loop. However, little is known about the specific molecules Prochlorococcus accumulates and releases or how these processes vary among its ecotypes. Here, we characterize the metabolite diversity of Prochlorococcus by profiling three ecologically distinct cultured strains: MIT9301, representing a high-light-adapted ecotype dominating shallow tropical and sub-tropical waters; MIT0801, representing a low-light-adapted ecotype found throughout the euphotic zone; and MIT9313, representing a low-light-adapted ecotype relatively most abundant at the base of the euphotic zone. In both intracellular and extracellular metabolite profiles, we observe striking differences across strains in the accumulation and release of molecules, such as the DNA methylating agent S-adenosyl-methionine (intracellular) and the branched-chain amino acids (intracellular) and their precursors (extracellular). While some differences reflect variable genome content across the strains, others likely reflect variable regulation of conserved pathways. In the extracellular profiles, we identify molecules such as pantothenic acid and aromatic amino acids that may serve as currencies in Prochlorococcus’ interactions with neighboring microbes and, therefore, merit further investigation. IMPORTANCE Approximately half of the annual carbon fixation on Earth occurs in the surface ocean through the photosynthetic activities of phytoplankton such as the ubiquitous picocyanobacterium Prochlorococcus. Ecologically distinct subpopulations (or ecotypes) of Prochlorococcus are central conduits of organic substrates into the ocean microbiome, thus playing important roles in surface ocean production. We measured the chemical profile of three cultured ecotype strains, observing striking differences among them that have implications for the likely chemical impact of Prochlorococcus subpopulations on their surroundings in the wild. Subpopulations differ in abundance along gradients of temperature, light, and nutrient concentrations, suggesting that these chemical differences could affect carbon cycling in different ocean strata and should be considered in models of Prochlorococcus physiology and marine carbon dynamics. |
| first_indexed | 2024-03-11T07:58:34Z |
| format | Article |
| id | doaj.art-3623df1e2a174cadb1b7d7d591e2a82e |
| institution | Directory Open Access Journal |
| issn | 2379-5077 |
| language | English |
| last_indexed | 2024-03-11T07:58:34Z |
| publishDate | 2023-10-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | mSystems |
| spelling | doaj.art-3623df1e2a174cadb1b7d7d591e2a82e2023-11-17T03:22:37ZengAmerican Society for MicrobiologymSystems2379-50772023-10-018510.1128/msystems.01261-22Metabolite diversity among representatives of divergent Prochlorococcus ecotypesElizabeth B. Kujawinski0Rogier Braakman1Krista Longnecker2Jamie W. Becker3Sallie W. Chisholm4Keven Dooley5Melissa C. Kido Soule6Gretchen J. Swarr7Kathryn Halloran8Department of Marine Chemistry and Geochemistry, Woods Hole Oceanographic Institution , Woods Hole, Massachusetts, USADepartment of Earth, Atmospheric, and Planetary Sciences, Massachusetts Institute of Technology , Cambridge, Massachusetts, USADepartment of Marine Chemistry and Geochemistry, Woods Hole Oceanographic Institution , Woods Hole, Massachusetts, USADepartment of Civil and Environmental Engineering, Massachusetts Institute of Technology , Cambridge, Massachusetts, USADepartment of Civil and Environmental Engineering, Massachusetts Institute of Technology , Cambridge, Massachusetts, USADepartment of Civil and Environmental Engineering, Massachusetts Institute of Technology , Cambridge, Massachusetts, USADepartment of Marine Chemistry and Geochemistry, Woods Hole Oceanographic Institution , Woods Hole, Massachusetts, USADepartment of Marine Chemistry and Geochemistry, Woods Hole Oceanographic Institution , Woods Hole, Massachusetts, USADepartment of Marine Chemistry and Geochemistry, Woods Hole Oceanographic Institution , Woods Hole, Massachusetts, USAABSTRACT The euphotic zone of the surface ocean contains distinct physical-chemical regimes that vary in light and nutrient concentrations as an inverse function of depth. The most numerous phytoplankter of the mid- and low-latitude ocean is the picocyanobacterium Prochlorococcus, which consists of ecologically distinct subpopulations (i.e., “ecotypes”). Ecotypes have different temperature, light, and nutrient optima and display distinct relative abundances along gradients of these niche dimensions. As a primary producer, Prochlorococcus fixes and releases organic carbon to neighboring microbes as part of the microbial loop. However, little is known about the specific molecules Prochlorococcus accumulates and releases or how these processes vary among its ecotypes. Here, we characterize the metabolite diversity of Prochlorococcus by profiling three ecologically distinct cultured strains: MIT9301, representing a high-light-adapted ecotype dominating shallow tropical and sub-tropical waters; MIT0801, representing a low-light-adapted ecotype found throughout the euphotic zone; and MIT9313, representing a low-light-adapted ecotype relatively most abundant at the base of the euphotic zone. In both intracellular and extracellular metabolite profiles, we observe striking differences across strains in the accumulation and release of molecules, such as the DNA methylating agent S-adenosyl-methionine (intracellular) and the branched-chain amino acids (intracellular) and their precursors (extracellular). While some differences reflect variable genome content across the strains, others likely reflect variable regulation of conserved pathways. In the extracellular profiles, we identify molecules such as pantothenic acid and aromatic amino acids that may serve as currencies in Prochlorococcus’ interactions with neighboring microbes and, therefore, merit further investigation. IMPORTANCE Approximately half of the annual carbon fixation on Earth occurs in the surface ocean through the photosynthetic activities of phytoplankton such as the ubiquitous picocyanobacterium Prochlorococcus. Ecologically distinct subpopulations (or ecotypes) of Prochlorococcus are central conduits of organic substrates into the ocean microbiome, thus playing important roles in surface ocean production. We measured the chemical profile of three cultured ecotype strains, observing striking differences among them that have implications for the likely chemical impact of Prochlorococcus subpopulations on their surroundings in the wild. Subpopulations differ in abundance along gradients of temperature, light, and nutrient concentrations, suggesting that these chemical differences could affect carbon cycling in different ocean strata and should be considered in models of Prochlorococcus physiology and marine carbon dynamics.https://journals.asm.org/doi/10.1128/msystems.01261-22ProchlorococcusmetabolomicsDNA methylation |
| spellingShingle | Elizabeth B. Kujawinski Rogier Braakman Krista Longnecker Jamie W. Becker Sallie W. Chisholm Keven Dooley Melissa C. Kido Soule Gretchen J. Swarr Kathryn Halloran Metabolite diversity among representatives of divergent Prochlorococcus ecotypes mSystems Prochlorococcus metabolomics DNA methylation |
| title | Metabolite diversity among representatives of divergent Prochlorococcus ecotypes |
| title_full | Metabolite diversity among representatives of divergent Prochlorococcus ecotypes |
| title_fullStr | Metabolite diversity among representatives of divergent Prochlorococcus ecotypes |
| title_full_unstemmed | Metabolite diversity among representatives of divergent Prochlorococcus ecotypes |
| title_short | Metabolite diversity among representatives of divergent Prochlorococcus ecotypes |
| title_sort | metabolite diversity among representatives of divergent prochlorococcus ecotypes |
| topic | Prochlorococcus metabolomics DNA methylation |
| url | https://journals.asm.org/doi/10.1128/msystems.01261-22 |
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