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Journal Article

Marine Proteobacteria metabolize glycolate via the β-hydroxyaspartate cycle

MPS-Authors
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Schada v. Borzyskowsi,  Lennart
Understanding and Building Metabolism, Department of Biochemistry and Synthetic Metabolism, Max Planck Institute for Terrestrial Microbiology, Max Planck Society;

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Severi,  Francesca
Understanding and Building Metabolism, Department of Biochemistry and Synthetic Metabolism, Max Planck Institute for Terrestrial Microbiology, Max Planck Society;

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Pommerenke,  B.
Understanding and Building Metabolism, Department of Biochemistry and Synthetic Metabolism, Max Planck Institute for Terrestrial Microbiology, Max Planck Society;

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Claus,  Peter
Understanding and Building Metabolism, Department of Biochemistry and Synthetic Metabolism, Max Planck Institute for Terrestrial Microbiology, Max Planck Society;
Core Facility Metabolics and small Molecules Mass Spectrometry, Max Planck Institute for Terrestrial Microbiology, Max Planck Society;

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Cortina,  Nina Socorro
Understanding and Building Metabolism, Department of Biochemistry and Synthetic Metabolism, Max Planck Institute for Terrestrial Microbiology, Max Planck Society;
Core Facility Metabolics and small Molecules Mass Spectrometry, Max Planck Institute for Terrestrial Microbiology, Max Planck Society;

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Glatter,  Timo
Core Facility Mass Spectrometry and Proteomics, Max Planck Institute for Terrestrial Microbiology, Max Planck Society;

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Zarzycki,  Jan
Understanding and Building Metabolism, Department of Biochemistry and Synthetic Metabolism, Max Planck Institute for Terrestrial Microbiology, Max Planck Society;

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Fuchs,  Bernhard M.
Department of Molecular Ecology, Max Planck Institute for Marine Microbiology, Max Planck Society;

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Erb,  Tobias J.
Understanding and Building Metabolism, Department of Biochemistry and Synthetic Metabolism, Max Planck Institute for Terrestrial Microbiology, Max Planck Society;

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Citation

Schada v. Borzyskowsi, L., Severi, F., Krueger, K., Hermann, L., Gilardet, A., Sippel, F., et al. (2019). Marine Proteobacteria metabolize glycolate via the β-hydroxyaspartate cycle. NATURE, 575(7783), 500-+. doi:10.1038/s41586-019-1748-4.


Cite as: https://hdl.handle.net/21.11116/0000-0008-BEE0-5
Abstract
One of the most abundant sources of organic carbon in the ocean is
glycolate, the secretion of which by marine phytoplankton results in an
estimated annual flux of one petagram of glycolate in marine
environments(1). Although it is generally accepted that glycolate is
oxidized to glyoxylate by marine bacteria(2-4), the further fate of this
C-2 metabolite is not well understood. Here we show that ubiquitous
marine Proteobacteria are able to assimilate glyoxylate via the
beta-hydroxyaspartate cycle (BHAC) that was originally proposed 56 years
ago(5). We elucidate the biochemistry of the BHAC and describe the
structure of its key enzymes, including a previously unknown primary
imine reductase. Overall, the BHAC enables the direct production of
oxaloacetate from glyoxylate through only four enzymatic steps,
representing-to our knowledge-the most efficient glyoxylate assimilation
route described to date. Analysis of marine metagenomes shows that the
BHAC is globally distributed and on average 20-fold more abundant than
the glycerate pathway, the only other known pathway for net glyoxylate
assimilation. In a field study of a phytoplankton bloom, we show that
glycolate is present in high nanomolar concentrations and taken up by
prokaryotes at rates that allow a full turnover of the glycolate pool
within one week. During the bloom, genes that encode BHAC key enzymes
are present in up to 1.5% of the bacterial community and actively
transcribed, supporting the role of the BHAC in glycolate assimilation
and suggesting a previously undescribed trophic interaction between
autotrophic phytoplankton and heterotrophic bacterioplankton.