Marine Proteobacteria metabolize glycolate via the β-hydroxyaspartate cycle

Borzyskowski, Lennart Schada von; Severi, Francesca; Krüger, Karen; Hermann, Lucas; Gilardet, Alexandre; Sippel, Felix; Pommerenke, Bianca; Claus, Peter; Cortina, Niña Socorro; Glatter, Timo; Zauner, Stefan; Zarzycki, Jan; Fuchs, Bernhard M.; Bremer, Erhard; Maier, Uwe G.; Amann, Rudolf; Erb, Tobias J.

doi:10.1038/s41586-019-1748-4

Cited by 83 publications

(89 citation statements)

References 75 publications

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“…Nevertheless, as analyzed comprehensively in SI Appendix , Supplementary Text , only a few other enzymes and pathways can potentially recycle glyoxylate, and even fewer of these are found in C. necator . For example, the β-hydroxyaspartate cycle was recently shown to enable growth on glycolate via glyoxylate assimilation ( 29 ), but the genome of C. necator does not encode its key glyoxylate assimilating enzyme, β-hydroxyaspartate aldolase. Of the very few metabolic pathways that might be involved in glyoxylate metabolism in C. necator ( SI Appendix , Supplementary Text ), the most plausible route relies on the enzyme malate synthase, a key component of the glyoxylate shunt that condenses glyoxylate with acetyl-CoA to generate malate ( 30 , 31 ).…”

Section: Resultsmentioning

confidence: 99%

Phosphoglycolate salvage in a chemolithoautotroph using the Calvin cycle

Claassens

Scarinci

Fischer

et al. 2020

Proc. Natl. Acad. Sci. U.S.A.

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Carbon fixation via the Calvin cycle is constrained by the side activity of Rubisco with dioxygen, generating 2-phosphoglycolate. The metabolic recycling of phosphoglycolate was extensively studied in photoautotrophic organisms, including plants, algae, and cyanobacteria, where it is referred to as photorespiration. While receiving little attention so far, aerobic chemolithoautotrophic bacteria that operate the Calvin cycle independent of light must also recycle phosphoglycolate. As the term photorespiration is inappropriate for describing phosphoglycolate recycling in these nonphotosynthetic autotrophs, we suggest the more general term “phosphoglycolate salvage.” Here, we study phosphoglycolate salvage in the model chemolithoautotroph Cupriavidus necator H16 (Ralstonia eutropha H16) by characterizing the proxy process of glycolate metabolism, performing comparative transcriptomics of autotrophic growth under low and high CO2 concentrations, and testing autotrophic growth phenotypes of gene deletion strains at ambient CO2. We find that the canonical plant-like C2 cycle does not operate in this bacterium, and instead, the bacterial-like glycerate pathway is the main route for phosphoglycolate salvage. Upon disruption of the glycerate pathway, we find that an oxidative pathway, which we term the malate cycle, supports phosphoglycolate salvage. In this cycle, glyoxylate is condensed with acetyl coenzyme A (acetyl-CoA) to give malate, which undergoes two oxidative decarboxylation steps to regenerate acetyl-CoA. When both pathways are disrupted, autotrophic growth is abolished at ambient CO2. We present bioinformatic data suggesting that the malate cycle may support phosphoglycolate salvage in diverse chemolithoautotrophic bacteria. This study thus demonstrates a so far unknown phosphoglycolate salvage pathway, highlighting important diversity in microbial carbon fixation metabolism.

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Section: Resultsmentioning

confidence: 99%

Phosphoglycolate salvage in a chemolithoautotroph using the Calvin cycle

Claassens

Scarinci

Fischer

et al. 2020

Proc. Natl. Acad. Sci. U.S.A.

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“…This positive feedback loop might also explain why P. tricornutum reached higher abundances in the condition with the methylamine mixture containing 0.66 mM MMA compared to the condition with the equimolar amount of MMA as the sole nitrogen source ( Figure 2A ). In this respect, glycolate, a frequent side product of algal assimilation from photorespiration ( Landa et al, 2017 ; Schada von Borzyskowski et al, 2019 ), could easily provide this function as an energy substrate in the phycosphere; in the case of strain KarMa, glycolate could only be used as an energy substrate. In agreement with this, the genome of strain KarMa contains the glycolate oxidase genes for dissimilating glycolate, but it lacks the gene for hydroxyaspartate aldolase, the key enzyme in the β-hydroxyaspartate cycle responsible for assimilating glycolate ( Schada von Borzyskowski et al, 2019 ).…”

Section: Discussionmentioning

confidence: 99%

Evidence of Interdomain Ammonium Cross-Feeding From Methylamine- and Glycine Betaine-Degrading Rhodobacteraceae to Diatoms as a Widespread Interaction in the Marine Phycosphere

2020

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Dissolved organic nitrogen (DON) compounds such as methylamines (MAs) and glycine betaine (GBT) occur at detectable concentrations in marine habitats and are also produced and released by microalgae. For many marine bacteria, these DON compounds can serve as carbon, energy, and nitrogen sources, but microalgae usually cannot metabolize them. Interestingly though, it was previously shown that Donghicola sp. strain KarMa—a member of the marine Rhodobacteraceae —can cross-feed ammonium such that the ammonium it produces upon degrading monomethylamine (MMA) then serves as nitrogen source for the diatom Phaeodactylum tricornutum ; thus, these organisms form a mutual metabolic interaction under photoautotrophic conditions. In the present study, we investigated whether this interaction plays a broader role in bacteria–diatom interactions in general. Results showed that cross-feeding between strain KarMa and P. tricornutum was also possible with di- and trimethylamine as well as with GBT. Further, cross-feeding of strain KarMa was also observed in cocultures with the diatoms Amphora coffeaeformis and Thalassiosira pseudonana with MMA as the sole nitrogen source. Regarding cross-feeding involving other Rhodobacteraceae strains, the in silico analysis of MA and GBT degradation pathways indicated that algae-associated Rhodobacteraceae -type strains likely interact with P. tricornutum in a similar manner as the strain KarMa does. For these types of strains (such as Celeribacter halophilus , Roseobacter denitrificans , Roseovarius indicus , Ruegeria pomeroyi , and Sulfitobacter noctilucicola ), ammonium cross-feeding after methylamine degradation showed species-specific patterns, whereas bacterial GBT degradation always led to diatom growth. Overall, the degradation of DON compounds by the Rhodobacteraceae family and the subsequent cross-feeding of ammonium may represent a widespread, organism-specific, and regulated metabolic interaction for establishing and stabilizing associations with photoautotrophic diatoms in the oceans.

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“…Both the glycerate pathway (Hansen and Hayashi 1962;Krakow and Barkulis 1956) and the β-hydroxyaspartate cycle (BHAC) (Kornberg and Morris 1963) were first investigated in the 1950s/60s. However, while glyoxylate carboligase and tartronate semialdehyde reductase, the key enzymes of the glycerate pathway, were identified quickly, probably because they are encoded by the model organism E. coli (Gotto and Kornberg 1961;Gupta and Vennesland 1964), the BHAC and its key enzyme iminosuccinate reductase were fully described only in 2019 (Schada von Borzyskowski et al 2019). Both of these pathways funnel two molecules of glyoxylate into central metabolism.…”

Section: Functional Degeneracy In Acetyl-coa Assimilation In Bacteriamentioning

confidence: 99%

“…However, the thermodynamic profile for the glycerate pathway is more favorable under standard conditions than for the BHAC, driving the pathway efficiently towards assimilation (Figure 4c). While marker genes of the BHAC are almost 20-fold more abundant in marine metagenomes than marker genes of the glycerate pathway (Schada von Borzyskowski et al 2019), the latter metabolic route seems to be more prevalent in bacterial isolates in general (Figure 4d).…”

Section: Functional Degeneracy In Acetyl-coa Assimilation In Bacteriamentioning

confidence: 99%

Biochemical unity revisited: microbial central carbon metabolism holds new discoveries, multi-tasking pathways, and redundancies with a reason

Borzyskowski

Bernhardsgrütter

Erb

2020

Biological Chemistry

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For a long time, our understanding of metabolism has been dominated by the idea of biochemical unity, i.e., that the central reaction sequences in metabolism are universally conserved between all forms of life. However, biochemical research in the last decades has revealed a surprising diversity in the central carbon metabolism of different microorganisms. Here, we will embrace this biochemical diversity and explain how genetic redundancy and functional degeneracy cause the diversity observed in central metabolic pathways, such as glycolysis, autotrophic CO2 fixation, and acetyl-CoA assimilation. We conclude that this diversity is not the exception, but rather the standard in microbiology.

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Marine Proteobacteria metabolize glycolate via the β-hydroxyaspartate cycle

Cited by 83 publications

References 75 publications

Phosphoglycolate salvage in a chemolithoautotroph using the Calvin cycle

Phosphoglycolate salvage in a chemolithoautotroph using the Calvin cycle

Evidence of Interdomain Ammonium Cross-Feeding From Methylamine- and Glycine Betaine-Degrading Rhodobacteraceae to Diatoms as a Widespread Interaction in the Marine Phycosphere

Biochemical unity revisited: microbial central carbon metabolism holds new discoveries, multi-tasking pathways, and redundancies with a reason

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