Metabolomics-derived marker metabolites to characterize Phaeocystis pouchetii physiology in natural plankton communities

Kuhlisch, Constanze; Althammer, Julia; Sazhin, Andrey F.; Jakobsen, Hans Henrik; Nejstgaard, Jens C.; Pohnert, Georg

doi:10.1038/s41598-020-77169-w

Cited by 13 publications

(3 citation statements)

References 77 publications

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“…The comprehensive analysis of the metabolites in a system (metabolomics) is a nascent field and analytically challenging in environmental settings (15)(16)(17). Metabolomic studies are being used to investigate physiological changes in marine organisms under laboratory conditions (4,(18)(19)(20)(21)(22), though the same techniques have only recently been applied to whole communities in natural environments (22). Existing community marine metabolomic studies have employed targeted approaches in which the compounds detected are chosen by the analyst (5,12,21,23,24) or the analytical techniques employed preclude the observation of small, highly polar compounds (25,26).…”

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confidence: 99%

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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Marine Community Metabolomes Carry Fingerprints of Phytoplankton Community Composition

et al. 2021

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“…Intracellular concentrations of mannitol paralleled increases in salinity in Tetraselmis chui , suggesting that it was involved in osmoregulation ( 30 ). Natural blooms of Phaeocystis pouchetii have endometabolomic profiles that include mannitol ( 31 ). The coccolithophore, Chrysotila dentate , has attached and free-living bacteria (mainly α-proteobacteria and γ-proteobacteria), which can use mannitol ( 32 ).…”

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confidence: 99%

Osmotrophy of dissolved organic compounds by coccolithophore populations: Fixation into particulate organic and inorganic carbon

et al. 2023

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Coccolithophores are typically thought of as photoautotrophs, yet a few genera inhabit sub-euphotic environments with insufficient light for photosynthesis, suggesting that other carbon acquisition strategies are likely. Field experiments were performed in the northwest Atlantic (a region with potentially abundant coccolithophores). Phytoplankton populations were incubated with 14 C-labeled dissolved organic carbon (DOC) compounds, acetate, mannitol, and glycerol. Coccolithophores were sorted from these populations 24 hours later using flow cytometry, and DOC uptake was measured. DOC uptake rates were as high as 10 −15 moles cell −1 day −1 , slow relative to photosynthesis rates (10 −12 moles cell −1 day −1 ). Growth rates on the organic compounds were low, suggesting that osmotrophy plays more of a survival strategy in low-light situations. Assimilated DOC was found in both particulate organic carbon and calcite coccoliths (particulate inorganic carbon), suggesting that osmotrophic uptake of DOC into coccolithophore calcite is a small but notable part of the biological carbon pump and alkalinity pump paradigms.

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“…When considering host control, which we tested by manipulating innate host selection microbiome bacterial community composition and diversity are known to change in function of the phytoplankton species, genotypes, bloom phase, and phytoplankton community composition indicating a potential role for phytoplankton host selection on their bacterial microbiome in natural systems (Cordone et al, 2022; Krohn‐Molt et al, 2017; Sison‐Mangus et al, 2016; Zhou et al, 2018). Further, phytoplankton metabolites composition varies between growth stages, where the exponential growth phase is marked by the presence of free amino acids while during the early stationary phase sugar alcohols, mono‐ and disaccharides are more abundant (Kuhlisch et al, 2020). These changes in phytoplankton‐derived metabolites can potentially affect its bacterial microbiome formation as well, as direct experimental evidence has shown that bacterial community composition can be predicted by the mixture of known phytoplankton exometabolites (Fu et al, 2020).…”

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confidence: 99%

Dissecting host‐microbiome interaction effects on phytoplankton microbiome composition and diversity

Yang,

Denef

2024

Environmental Microbiology

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Phytoplankton and their associated microbiomes of heterotrophic bacteria are foundational to primary production, energy transfer, and biogeochemical cycling in aquatic systems. While it is known that these microbiomes are shaped by host‐released dissolved organic matter (DOM), the extent to which dynamic phytoplankton‐bacteria interactions shape bacterial community assembly remains to be examined. Here, we investigated the effects of two mechanisms in host‐microbiome interactions on phytoplankton bacterial microbiome formation: (i) innate host selection and (ii) host‐microbiome feedback. For the former, phytoplankton‐produced DOM composition is based solely on the host's properties (species or physiological state); for the latter, the presence of the microbiome modifies host DOM production. The microbiome of Chlorella sorokiniana was extracted and exposed to six ratios of the two effects. We found that microbiome composition changed along with the six host‐microbiome feedback versus innate host selection ratios, with the highest compositional distance between communities under the strongest and the weakest ratio of the two effects. This indicates that each mechanism selects for different bacterial species. In addition, our findings showed that when both selective forces were applied, it led to a higher community richness, while host‐microbiome feedback alone reduces community evenness due to its strong species‐specific selection.

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Metabolomics-derived marker metabolites to characterize Phaeocystis pouchetii physiology in natural plankton communities

Cited by 13 publications

References 77 publications

Marine Community Metabolomes Carry Fingerprints of Phytoplankton Community Composition

Marine Community Metabolomes Carry Fingerprints of Phytoplankton Community Composition

Osmotrophy of dissolved organic compounds by coccolithophore populations: Fixation into particulate organic and inorganic carbon

Dissecting host‐microbiome interaction effects on phytoplankton microbiome composition and diversity

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