Ectoine from Bacterial and Algal Origin Is a Compatible Solute in Microalgae

Fenizia, Simona; Thume, Kathleen; Wirgenings, Marino; Pohnert, Georg

doi:10.3390/md18010042

Cited by 55 publications

(69 citation statements)

References 43 publications

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“…6D; see also Table S8 at https://doi.org/10.5061/dryad.brv15dv8s). Homarine has been observed in diatoms and E. huxleyi in previous studies (20,(41)(42)(43)(44)(45) but has not been associated with the ubiquitous marine cyanobacterium Synechococcus. We estimated that homarine was 4.8% of the particulate carbon within Synechococcus strain WH8102.…”

Section: Resultsmentioning

confidence: 80%

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Marine Community Metabolomes Carry Fingerprints of Phytoplankton Community Composition

et al. 2021

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Phytoplankton transform inorganic carbon into thousands of biomolecules that represent an important pool of fixed carbon, nitrogen, and sulfur in the surface ocean. Metabolite production differs between phytoplankton, and the flux of these molecules through the microbial food web depends on compound-specific bioavailability to members of a wider microbial community. Yet relatively little is known about the diversity or concentration of metabolites within marine plankton. Here, we compare 313 polar metabolites in 21 cultured phytoplankton species and in natural planktonic communities across environmental gradients to show that bulk community metabolomes reflect the chemical composition of the phytoplankton community. We also show that groups of compounds have similar patterns across space and taxonomy, suggesting that the concentrations of these compounds in the environment are controlled by similar sources and sinks. We quantify several compounds in the surface ocean that represent substantial understudied pools of labile carbon. For example, the N-containing metabolite homarine was up to 3% of particulate carbon and is produced in high concentrations by cultured Synechococcus, and S-containing gonyol accumulated up to 2.5 nM in surface particles and likely originates from dinoflagellates or haptophytes. Our results show that phytoplankton composition directly shapes the carbon composition of the surface ocean. Our findings suggest that in order to access these pools of bioavailable carbon, the wider microbial community must be adapted to phytoplankton community composition. IMPORTANCE Microscopic phytoplankton transform 100 million tons of inorganic carbon into thousands of different organic compounds each day. The structure of each chemical is critical to its biological and ecosystem function, yet the diversity of biomolecules produced by marine microbial communities remained mainly unexplored, especially small polar molecules which are often considered the currency of the microbial loop. Here, we explore the abundance and diversity of small biomolecules in planktonic communities across ecological gradients in the North Pacific and within 21 cultured phytoplankton species. Our work demonstrates that phytoplankton diversity is an important determinant of the chemical composition of the highly bioavailable pool of organic carbon in the ocean, and we highlight understudied yet abundant compounds in both the environment and cultured organisms. These findings add to understanding of how the chemical makeup of phytoplankton shapes marine microbial communities where the ability to sense and use biomolecules depends on the chemical structure.

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Section: Resultsmentioning

confidence: 80%

“…Samples for the NPSG depth profile were collected aboard the R.V. Kilo Moana cruise KM1513 on 31 July 2015 from four depths (15,45,75, and 125 m); we reported on these samples in a previous publication (16). Samples for the meridional transect were collected on cruise KOK1606 aboard the R.V.…”

Section: Methodsmentioning

confidence: 99%

Marine Community Metabolomes Carry Fingerprints of Phytoplankton Community Composition

et al. 2021

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“…In our cultured isolates, we detected homarine in both Synechococcus strains (intracellular concentration up to mM), four of six surveyed diatoms (0.5-57 mM) and one strain of Emiliania huxleyi (a haptophyte, at 3.8 mM, Figure 6D, Table S8). Homarine has been observed in diatoms and E. huxleyi in previous studies (20,40,41,42,43,44), but has not been associated with the ubiquitous marine cyanobacteria Synechococcus.…”

Section: Metabolites As a Quantitative Component Of The Bulk Carbonmentioning

confidence: 76%

Marine community metabolomes carry fingerprints of phytoplankton community composition

Durham

Boysen

Carlson

et al. 2020

Preprint

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Phytoplankton transform inorganic carbon into thousands of biomolecules that represent an important pool of fixed carbon, nitrogen, and sulfur in the surface ocean. Metabolite production differs between phytoplankton, and the flux of these molecules through the microbial food web depends on compound-specific bioavailability to members of a wider microbial community. Yet relatively little is known about the diversity or concentration of metabolites within marine plankton. Here we compare 313 polar metabolites in 21 cultured phytoplankton species and in natural planktonic communities across environmental gradients to show that bulk community metabolomes reflect chemical composition of the phytoplankton community. We also show that groups of compounds have similar patterns across space and taxonomy suggesting that the concentrations of these compounds in the environment are controlled by similar sources and sinks. We quantify several compounds in the surface ocean that represent substantial understudied pools of labile carbon. For example, the N-containing metabolite homarine was up to 3% of particulate carbon and is produced in high concentrations by cultured Synechococcus, and S-containing gonyol accumulated up to 2.5 nM in surface particles and likely originates from dinoflagellates. Our results show that phytoplankton composition directly shapes the carbon composition of the surface ocean. Our findings suggest that in order to access these pools of bioavailable carbon, the wider microbial community must be adapted to phytoplankton community composition.IMPORTANCEMicroscopic phytoplankton transform 100 million tons of inorganic carbon into thousands of different organic compounds each day. The structure of each chemical is critical to its biological and ecosystem function, yet, the diversity of biomolecules produced by marine microbial communities remained mainly unexplored, especially small polar molecules which are often considered the currency of the microbial loop. Here we explore the abundance and diversity of small biomolecules in planktonic communities across ecological gradients in the North Pacific and within 21 cultured phytoplankton species. Our work demonstrates that phytoplankton diversity is an important determinant of the chemical composition of the highly bioavailable pool of organic carbon in the ocean, and we highlight understudied yet abundant compounds in both the environment and cultured organisms. These findings add to understanding of how the chemical makeup of phytoplankton shapes marine microbial communities where the ability to sense and use biomolecules depends on the chemical structure.

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“…Severely osmotically stressed microorganisms synthesize and accumulate ectoines to cellular concentrations as high as hundreds of micromolar. The recent exiting discovery of ectoine production and uptake by halophilic protists and marine microalgae (55)(56)(57) raises the possibility for ectoines to function in microbial interactions with these eukaryotic cells. Similarly to the catabolism of the compatible solutes DMSP, choline, and glycine betaine, their environmental release can shape architecture and composition of microbial communities (57,58).…”

Section: Discussionmentioning

confidence: 99%

Degradation of the microbial stress protectants and chemical chaperones ectoine and hydroxyectoine by a bacterial hydrolase–deacetylase complex

Mais

Hermann

Altegoer

et al. 2020

Journal of Biological Chemistry

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When faced with increased osmolarity in the environment, many bacterial cells accumulate the compatible solute ectoine and its derivative 5-hydroxyectoine. Both compounds are not only potent osmostress protectants, but also serve as effective chemical chaperones stabilizing protein functionality. Ectoines are energy-rich nitrogen and carbon sources that have an ecological impact that shapes microbial communities. Although the biochemistry of ectoine and 5-hydroxyectoine biosynthesis is well understood, our understanding of their catabolism is only rudimentary. Here, we combined biochemical and structural approaches to unravel the core of ectoine and 5-hydroxy-ectoine catabolisms. We show that a conserved enzyme bimodule consisting of the EutD ectoine/5-hydroxyectoine hydrolase and the EutE deacetylase degrades both ectoines. We determined the high-resolution crystal structures of both enzymes, derived from the salt-tolerant bacteria Ruegeria pomeroyi and Halomonas elongata. These structures, either in their apo-forms or in forms capturing substrates or intermediates, provided detailed insights into the catalytic cores of the EutD and EutE enzymes. The combined biochemical and structural results indicate that the EutD homodimer opens the pyrimidine ring of ectoine through an unusual covalent intermediate, N-α-2 acetyl-l-2,4-diaminobutyrate (α-ADABA). We found that α-ADABA is then deacetylated by the zinc-dependent EutE monomer into diaminobutyric acid (DABA), which is further catabolized to l-aspartate. We observed that the EutD–EutE bimodule synthesizes exclusively the α-, but not the γ-isomers of ADABA or hydroxy–ADABA. Of note, α-ADABA is known to induce the MocR/GabR-type repressor EnuR, which controls the expression of many ectoine catabolic genes clusters. We conclude that hydroxy–α-ADABA might serve a similar function.

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Ectoine from Bacterial and Algal Origin Is a Compatible Solute in Microalgae

Cited by 55 publications

References 43 publications

Marine Community Metabolomes Carry Fingerprints of Phytoplankton Community Composition

Marine Community Metabolomes Carry Fingerprints of Phytoplankton Community Composition

Marine community metabolomes carry fingerprints of phytoplankton community composition

Degradation of the microbial stress protectants and chemical chaperones ectoine and hydroxyectoine by a bacterial hydrolase–deacetylase complex

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