Novel bacterial clade reveals origin of form I Rubisco

Banda, Douglas M.; Pereira, J.H.; Liu, Albert K; Orr, Douglas J.; Hammel, Michal; He, Christine; Parry, M. A. J.; Carmo‐Silva, Elizabete; Adams, Paul D.; Banfield, Jillian F.; Shih, Patrick M.

doi:10.1038/s41477-020-00762-4

Cited by 62 publications

(87 citation statements)

References 76 publications

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“…2008 ), whereas Form II, III, and IV rubisco found in other lineages are comprised of just the large subunit ( Tabita et al. 2008 ; Banda et al. 2020 ).…”

Section: Introductionmentioning

confidence: 99%

Rubisco Adaptation Is More Limited by Phylogenetic Constraint Than by Catalytic Trade-off

Bouvier

Emms

Rhodes

et al. 2021

Molecular Biology and Evolution

127

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Rubisco assimilates CO2 to form the sugars that fuel life on earth. Correlations between rubisco kinetic traits across species have led to the proposition that rubisco adaptation is highly constrained by catalytic trade-offs. However, these analyses did not consider the phylogenetic context of the enzymes that were analysed. Thus, it is possible that the correlations observed were an artefact of the presence of phylogenetic signal in rubisco kinetics and the phylogenetic relationship between the species that were sampled. Here, we conducted a phylogenetically-resolved analysis of rubisco kinetics and show that there is a significant phylogenetic signal in rubisco kinetic traits. We re-evaluated the extent of catalytic trade-offs accounting for this phylogenetic signal and found that all were attenuated. Following phylogenetic correction, the largest catalytic trade-offs were observed between the Michaelis constant for CO2 and carboxylase turnover (∼21-37%), and between the Michaelis constants for CO2 and O2 (∼9-19%), respectively. All other catalytic trade-offs were substantially attenuated such that they were marginal (<9%) or non-significant. This phylogenetically resolved analysis of rubisco kinetic evolution also identified kinetic changes that occur concomitant with the evolution of C4 photosynthesis. Finally, we show that phylogenetic constraints have played a larger role than catalytic trade-offs in limiting the evolution of rubisco kinetics. Thus, although there is strong evidence for some catalytic trade-offs, rubisco adaptation has been more limited by phylogenetic constraint than by the combined action of all such trade-offs.

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“…2008 ), whereas Form II, III, and IV rubisco found in other lineages are comprised of just the large subunit ( Tabita et al. 2008 ; Banda et al. 2020 ).…”

Section: Introductionmentioning

confidence: 99%

Rubisco Adaptation Is More Limited by Phylogenetic Constraint Than by Catalytic Trade-off

Bouvier

Emms

Rhodes

et al. 2021

Molecular Biology and Evolution

127

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“…However, in many cases, such dimers may form higher-level oligomers, which help to pack more molecules in the available space, increasing net CO 2 assimilation. Formation of an octamer is important for higher plant Rubiscos (form I), as well as the recently described form I' (lacking the small subunit) from Anaerolineales [28]. Interestingly, some residues with potential to improve CO 2 fixation were identified in the oligomerization interface of Thermosynechococcus elongatus Rubisco [29].…”

Section: Oligomerization Interface Analysismentioning

confidence: 99%

Insights into the Structure of Rubisco from Dinoflagellates-In Silico Studies

Rydzy

Tracz

Szczepaniak

et al. 2021

IJMS

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Ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco) is one of the best studied enzymes. It is crucial for photosynthesis, and thus for all of biosphere’s productivity. There are four isoforms of this enzyme, differing by amino acid sequence composition and quaternary structure. However, there is still a group of organisms, dinoflagellates, single-cell eukaryotes, that are confirmed to possess Rubisco, but no successful purification of the enzyme of such origin, and hence a generation of a crystal structure was reported to date. Here, we are using in silico tools to generate the possible structure of Rubisco from a dinoflagellate representative, Symbiodinium sp. We selected two templates: Rubisco from Rhodospirillum rubrum and Rhodopseudomonas palustris. Both enzymes are the so-called form II Rubiscos, but the first is exclusively a homodimer, while the second one forms homo-hexamers. Obtained models show no differences in amino acids crucial for Rubisco activity. The variation was found at two closely located inserts in the C-terminal domain, of which one extends a helix and the other forms a loop. These inserts most probably do not play a direct role in the enzyme’s activity, but may be responsible for interaction with an unknown protein partner, possibly a regulator or a chaperone. Analysis of the possible oligomerization interface indicated that Symbiodinium sp. Rubisco most likely forms a trimer of homodimers, not just a homodimer. This hypothesis was empowered by calculation of binding energies. Additionally, we found that the protein of study is significantly richer in cysteine residues, which may be the cause for its activity loss shortly after cell lysis. Furthermore, we evaluated the influence of the loop insert, identified exclusively in the Symbiodinium sp. protein, on the functionality of the recombinantly expressed R. rubrum Rubisco. All these findings shed new light onto dinoflagellate Rubisco and may help in future obtainment of a native, active enzyme.

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“…An interesting recent report demonstrated the genomic capacity for production of photosynthetic reaction centers in the Chloroflexota order Aggregatilineales, within the clade Anaerolinea, based on the presence of divergent pufLM-like reaction centers [12] . Some representatives of the Chloroflexi supergroup have the ability for chemoautotrophic fixation of CO 2 [13] , oxidation of CO [14] [16] , and oxidation of H 2 [16] [17] . A surprising and interesting recent finding is that bacteria within Chloroflexota class Anaerolinea have Form I Rubisco sequences which form a clade that is clearly basal to previously known Form I Rubiscos.…”

Section: Introductionmentioning

confidence: 99%

The Chloroflexi supergroup is metabolically diverse and representatives have novel genes for non-photosynthesis based CO₂ fixation

West-Roberts

Carnevali

Schoelmerich

et al. 2021

Preprint

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The Chloroflexi superphylum have been investigated primarily from the perspective of reductive dehalogenation of toxic compounds, anaerobic photosynthesis and wastewater treatment, but remain relatively little studied compared to their close relatives within the larger Terrabacteria group, including Cyanobacteria, Actinobacteria, and Firmicutes. Here, we conducted a detailed phylogenetic analysis of the phylum Chloroflexota, the phylogenetically proximal candidate phylum Dormibacteraeota, and a newly defined sibling phylum proposed in the current study, Eulabeiota. These groups routinely root together in phylogenomic analyses, and constitute the Chloroflexi supergroup. Chemoautotrophy is widespread in Chloroflexi. Two Form I Rubisco ancestral subtypes that both lack the small subunit are prevalent in ca. Eulabeiota and Chloroflexota, suggesting that the predominant modern pathway for CO2 fixation evolved in these groups. The single subunit Form I Rubiscos are inferred to have evolved prior to oxygenation of the Earth's atmosphere and now predominantly occur in anaerobes. Prevalent in both Chloroflexota and ca. Eulabeiota are capacities related to aerobic oxidation of gases, especially CO and H2. In fact, aerobic and anaerobic CO dehydrogenases are widespread throughout every class-level lineage, whereas traits such as denitrification and reductive dehalogenation are heterogeneously distributed across the supergroup. Interestingly, some Chloroflexota have a novel clade of group 3 NiFe hydrogenases that is phylogenetically distinct from previously reported groups. Overall, the analyses underline the very high level of metabolic diversity in the Chloroflexi supergroup, suggesting the ancestral metabolic platform for this group enabled highly varied adaptation to ecosystems that appeared in the aerobic world.

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Novel bacterial clade reveals origin of form I Rubisco

Cited by 62 publications

References 76 publications

Rubisco Adaptation Is More Limited by Phylogenetic Constraint Than by Catalytic Trade-off

Rubisco Adaptation Is More Limited by Phylogenetic Constraint Than by Catalytic Trade-off

Insights into the Structure of Rubisco from Dinoflagellates-In Silico Studies

The Chloroflexi supergroup is metabolically diverse and representatives have novel genes for non-photosynthesis based CO₂ fixation

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Novel bacterial clade reveals origin of form I Rubisco

Cited by 62 publications

References 76 publications

Rubisco Adaptation Is More Limited by Phylogenetic Constraint Than by Catalytic Trade-off

Rubisco Adaptation Is More Limited by Phylogenetic Constraint Than by Catalytic Trade-off

Insights into the Structure of Rubisco from Dinoflagellates-In Silico Studies

The Chloroflexi supergroup is metabolically diverse and representatives have novel genes for non-photosynthesis based CO2 fixation

Contact Info

Product

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The Chloroflexi supergroup is metabolically diverse and representatives have novel genes for non-photosynthesis based CO₂ fixation