SAR11 Cells Rely on Enzyme Multifunctionality To Metabolize a Range of Polyamine Compounds

Noell, Stephen E.; Barrell, Gregory E.; Suffridge, Christopher; Morré, Jeff; Gable, Kevin P.; Graff, Jason R.; VerWey, Brian J.; Hellweger, Ferdi L.; Giovannoni, Stephen J.

doi:10.1128/mbio.01091-21

Cited by 15 publications

(10 citation statements)

References 83 publications

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“…Excess uptake and storage of GBT may be a strategy for surviving patchy and nutrient‐limited regions of the ocean. Similar luxury uptake strategies have been proposed for inorganic nutrients and other organic nutrients, including uptake of polyamines by SAR11 (Gaubert et al ., 2020; Noell et al ., 2021). Future studies of organisms in culture should explore this potential use of GBT and other nitrogen‐containing osmolytes as a mechanism for increased fitness in low and fluctuating nitrogen regimes.…”

Section: Resultsmentioning

confidence: 99%

Glycine betaine uptake and metabolism in marine microbial communities

Boysen

Durham

Kumler

et al. 2022

Environmental Microbiology

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Summary Glycine betaine (GBT) is a compatible solute in high concentrations in marine microorganisms. As a component of labile organic matter, GBT has complex biochemical potential as a substrate for microbial use that is unconstrained in the environment. Here we determine the uptake kinetics and metabolic fate of GBT in two natural microbial communities in the North Pacific characterized by different nitrate concentrations. Dissolved GBT had maximum uptake rates of 0.36 and 0.56 nM h−1 with half‐saturation constants of 79 and 11 nM in the high nitrate and low nitrate stations respectively. During multiday incubations, most GBT taken into cells was retained as a compatible solute. Stable isotopes derived from the added GBT were also observed in other metabolites, including choline, carnitine and sarcosine, suggesting that GBT was used for biosynthesis and for catabolism to pyruvate and ammonium. Where nitrate was scarce, GBT was primarily metabolized via demethylation to glycine. Gene transcript data were consistent with SAR11 using GBT as a source of methyl groups to fuel the methionine cycle. Where nitrate concentrations were higher, more GBT was partitioned for lipid biosynthesis by both bacteria and eukaryotic phytoplankton. Our data highlight unexpected metabolic pathways and potential routes of microbial metabolite exchange.

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Section: Resultsmentioning

confidence: 99%

Glycine betaine uptake and metabolism in marine microbial communities

Boysen

Durham

Kumler

et al. 2022

Environmental Microbiology

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“…SAR11 and some AEGEAN-169 members have homologs of the potABCD spermidine/putrescine ABC transporter (Supplemental Information -https://doi.org/10.6084/m9.figshare.22027763), and SAR11 responds disproportionately to addition of both of these polyamines in natural communities (87, 88). The potABCD genes transport five different polyamines in SAR11, where these compounds can meet cellular nitrogen requirements (89), and is spermidine-preferential in Escherichia coli (90). The additional potFGHI genes in AEGEAN-169 suggest increased use of putrescine compared to SAR11, as this transporter is considered putrescine-specific (90).…”

Section: Discussionmentioning

confidence: 99%

The AEGEAN-169 clade of bacterioplankton is synonymous with SAR11 subclade V (HIMB59) and metabolically distinct

Getz

Lanclos

Kojima

et al. 2023

Preprint

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Bacterioplankton of the SAR11 clade are the most abundant marine microorganisms and consist of numerous subclades spanning Order level divergence (Pelagibacterales). The assignment of the earliest diverging subclade V (a.k.a. HIMB59) to thePelagibacteralesis highly controversial, with multiple recent phylogenetic studies placing them completely separate from SAR11. Other than through phylogenomics, subclade V has not received detailed examination due to limited genomes from this group. Here, we assessed the ecogenomic characteristics of subclade V to better understand the role of this group in comparison to thePelagibacterales. We used a new isolate genome, recently released single amplified genomes (SAGs) and metagenome-assembled genomes (MAGs), and previously established SAR11 genomes to perform a comprehensive comparative genomics analysis. We paired this analysis with recruitment of metagenomes spanning open ocean, coastal, and brackish systems. Phylogenomics, average amino acid identity, and 16S rRNA gene phylogeny indicate that SAR11 subclade V is synonymous with the ubiquitous AEGEAN-169 clade, and support the contention that this group represents a taxonomic Family. AEGEAN-169 shared many bulk genome qualities with SAR11, such as streamlining and low GC content, but genomes were generally larger. AEGEAN-169 had overlapping distributions with SAR11 but was metabolically distinct from SAR11 in its potential to transport and utilize a broader range of sugars as well as in transport of trace metals and thiamin. Thus, regardless of the ultimate phylogenetic placement of AEGEAN-169, these organisms have distinct metabolic capacities that likely allow them to differentiate their niche from canonical SAR11 taxa.

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“…acting only on methylthioadenosine) than we hypothesize here, but this enzyme is known to act on multiple substrates in other microbial systems, including as part of the pathway we identify here (25,26). Enzyme multi-functionality is generally thought to be an important strategy in bacteria with streamlined genomes like Prochlorococcus (27,28). A lack of other identifiable pathways thus leads us to tentatively conclude that thymidine, adenine and guanine are all intermediates or endpoints of a shared, broad specificity deoxyribonucleotide recycling pathway (Fig.…”

Section: Resultsmentioning

confidence: 99%

Global niche partitioning of purine and pyrimidine cross-feeding among ocean microbes

Braakman,

Satinsky,

O'Keefe

et al. 2024

Preprint

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Characterizing the diversity of cross-feeding pathways in ocean microbes illuminates forces shaping co-evolution, ecosystem self-assembly and carbon cycling. Here we uncover a purine and pyrimidine cross-feeding network in globally abundant groups. The cyanobacterium Prochlorococcus exudes both compound classes, which metabolic reconstructions suggest follows synchronous daily genome replication. Co-occurring heterotrophs differentiate into purine or pyrimidine specialists, or generalists, and use compounds for different purposes. The most abundant heterotroph, SAR11, is a specialist that uses purines as sources of energy, carbon and/or nitrogen, with subgroups differentiating along ocean-scale gradients in the supply of energy and nitrogen, in turn leading to putative cryptic nitrogen cycles that link many microbes. Finally, in a SAR11 subgroup that dominates where Prochlorococcus is abundant, adenine additions to cultures inhibit DNA synthesis, poising cells for replication. We argue this subgroup uses inferred daily pulses of adenine from Prochlorococcus to metabolically synchronize to the daily supply of photosynthate from surrounding phytoplankton.

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SAR11 Cells Rely on Enzyme Multifunctionality To Metabolize a Range of Polyamine Compounds

Cited by 15 publications

References 83 publications

Glycine betaine uptake and metabolism in marine microbial communities

Glycine betaine uptake and metabolism in marine microbial communities

The AEGEAN-169 clade of bacterioplankton is synonymous with SAR11 subclade V (HIMB59) and metabolically distinct

Global niche partitioning of purine and pyrimidine cross-feeding among ocean microbes

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