Distinct form I, II, III, and IV Rubisco proteins from the three kingdoms of life provide clues about Rubisco evolution and structure/function relationships

Tabita, F. Robert; Satagopan, Sriram; Hanson, Thomas E.; Kreel, Nathan E.; Scott, Stephanie S.

doi:10.1093/jxb/erm361

Cited by 365 publications

(354 citation statements)

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“…This interpretation is consistent with previous phylogenetic analysis in which protein sequences of Rubisco Group I and Group III were inferred to form a monophyletic clade exclusive of Group II and IV (Tabita, Satagopan, et al., 2008). However, there exists an alternate hypothesis in which Group II—not Group III—is most closely related to Group I (Andersson & Backlund, 2008; Ashida et al., 2005).…”

Section: Discussionmentioning

confidence: 99%

“…Form I is a complex of eight large‐subunit dimers and eight small subunits and occurs in oxygenated environments. Form II is composed of individual dimers (comparable to the large Form I subunits) and is also found in organisms living in oxic environments such as the Proteobacteria and eukaryotic Alveolates (Tabita, Satagopan, Hanson, Kreel, & Scott, 2008). Form III is found mainly in anaerobic archaea (e.g., methanogenic and thermophilic crenarchaeota and some euryarchaeota) as either individual dimers or dimers arranged in a pentagonal array (Kitano et al., 2001).…”

Section: Introductionmentioning

confidence: 99%

“…This interpretation is consistent with models of a linear bacterial phylogeny in which Gram‐positive bacteria emerged earlier than Archaea, Gram‐negative bacteria or photosynthetic bacteria; organisms such as B. subtilis that use the methionine salvage pathway with Rubisco‐like proteins would have emerged before the evolutionary completion of the Calvin cycle and thus Rubisco's canonical role in CO 2 uptake (Gupta, 1998). Another interpretation of the available data from Rubisco and Rubisco‐like proteins posits that the most likely scenario was that a Form III Rubisco, arising within the Methanomicrobia, was the ultimate source of all Rubisco and RLP lineages (Tabita, 1999; Tabita, Hanson, Satagopan, Witte, & Kreel, 2008; Tabita, Satagopan, et al., 2008). Regardless of which part of the Rubisco protein family network emerged first, the ancestral path of Form I is the most conducive to calibration with the Precambrian fossil record over a span of time that includes the emergence of significant amounts of oxygen in the Earth's atmosphere (Schopf, 2011).…”

Section: Introductionmentioning

confidence: 99%

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Constraining the timing of the Great Oxidation Event within the Rubisco phylogenetic tree

et al. 2017

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Ribulose 1,5‐bisphosphate (RuBP) carboxylase/oxygenase (RuBisCO, or Rubisco) catalyzes a key reaction by which inorganic carbon is converted into organic carbon in the metabolism of many aerobic and anaerobic organisms. Across the broader Rubisco protein family, homologs exhibit diverse biochemical characteristics and metabolic functions, but the evolutionary origins of this diversity are unclear. Evidence of the timing of Rubisco family emergence and diversification of its different forms has been obscured by a meager paleontological record of early Earth biota, their subcellular physiology and metabolic components. Here, we use computational models to reconstruct a Rubisco family phylogenetic tree, ancestral amino acid sequences at branching points on the tree, and protein structures for several key ancestors. Analysis of historic substitutions with respect to their structural locations shows that there were distinct periods of amino acid substitution enrichment above background levels near and within its oxygen‐sensitive active site and subunit interfaces over the divergence between Form III (associated with anoxia) and Form I (associated with oxia) groups in its evolutionary history. One possible interpretation is that these periods of substitutional enrichment are coincident with oxidative stress exerted by the rise of oxygenic photosynthesis in the Precambrian era. Our interpretation implies that the periods of Rubisco substitutional enrichment inferred near the transition from anaerobic Form III to aerobic Form I ancestral sequences predate the acquisition of Rubisco by fully derived cyanobacterial (i.e., dual photosystem‐bearing, oxygen‐evolving) clades. The partitioning of extant lineages at high clade levels within our Rubisco phylogeny indicates that horizontal transfer of Rubisco is a relatively infrequent event. Therefore, it is possible that the mutational enrichment periods between the Form III and Form I common ancestral sequences correspond to the adaptation of key oxygen‐sensitive components of Rubisco prior to, or coincident with, the Great Oxidation Event.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Constraining the timing of the Great Oxidation Event within the Rubisco phylogenetic tree

et al. 2017

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“…Most of our understanding of RubisCO functioning is based on the studies conducted with cultured bacteria (Joshi et al, 2009 and references therein; Tabita et al, 2008 and references therein), but hardly any information exists about the function of environmental RubisCOs and the role of the enzymes encoded on the flanking DNA regions. Approaches that are currently used for gathering information on environmental RubisCO gene clusters rely on sequence searches (for example, Xie et al, 2011).…”

Section: Introductionmentioning

confidence: 99%

A function-based screen for seeking RubisCO active clones from metagenomes: novel enzymes influencing RubisCO activity

Böhnke

Perner

2014

The ISME Journal

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Ribulose-1,5-bisphosphate carboxylase/oxygenase (RubisCO) is a key enzyme of the Calvin cycle, which is responsible for most of Earth's primary production. Although research on RubisCO genes and enzymes in plants, cyanobacteria and bacteria has been ongoing for years, still little is understood about its regulation and activation in bacteria. Even more so, hardly any information exists about the function of metagenomic RubisCOs and the role of the enzymes encoded on the flanking DNA owing to the lack of available function-based screens for seeking active RubisCOs from the environment. Here we present the first solely activity-based approach for identifying RubisCO active fosmid clones from a metagenomic library. We constructed a metagenomic library from hydrothermal vent fluids and screened 1056 fosmid clones. Twelve clones exhibited RubisCO activity and the metagenomic fragments resembled genes from Thiomicrospira crunogena. One of these clones was further analyzed. It contained a 35.2 kb metagenomic insert carrying the RubisCO gene cluster and flanking DNA regions. Knockouts of twelve genes and two intergenic regions on this metagenomic fragment demonstrated that the RubisCO activity was significantly impaired and was attributed to deletions in genes encoding putative transcriptional regulators and those believed to be vital for RubisCO activation. Our new technique revealed a novel link between a poorly characterized gene and RubisCO activity. This screen opens the door to directly investigating RubisCO genes and respective enzymes from environmental samples.

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“…[NiFe]-hydrogenase, [MoCu]-carbon monoxide dehydrogenase, and RuBisCO enzymes encoded within the metagenome were classified by constructing phylogenetic trees of their catalytic subunits 21,49,50 . The derived protein sequences encoding the catalytic subunits of these enzymes were aligned with reference sequences reported in previous studies 21,49,50 using ClustalX 51 .…”

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confidence: 99%

Atmospheric trace gases support primary production in Antarctic desert surface soil

Greening

Vanwonterghem

et al. 2017

Nature

301

306

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Cultivation-independent surveys have shown that the desert soils of Antarctica harbour surprisingly rich microbial communities 1-3 . Given that phototroph abundance varies across these Antarctic soils 2,4 , an enduring question is what supports life in those communities with low photosynthetic capacity 3,5 . Here we provide evidence that atmospheric trace gases are the primary energy sources of two Antarctic surface soil communities. We reconstructed 23 draft genomes from metagenomic reads, including genomes from the candidate bacterial phyla WPS-2 and AD3. The dominant community members encoded and expressed high-affinity hydrogenases, carbon monoxide dehydrogenases, and a RuBisCO lineage known to support chemosynthetic carbon fixation 6,7 . Soil microcosms aerobically scavenged atmospheric H 2 and CO at rates sufficient to sustain their theoretical maintenance energy and mediated substantial levels of chemosynthetic but not photosynthetic CO 2 fixation. We propose that atmospheric H 2 , CO 2 and CO provide dependable sources of energy and carbon to support these communities, which suggests that atmospheric energy sources can provide an alternative basis for ecosystem function to solar or geological energy sources 8,9 . Although more extensive sampling is required to verify whether this process is widespread in terrestrial Antarctica and other oligotrophic habitats, our results provide new understanding of the minimal nutritional requirements for life and open the possibility that atmospheric gases support life on other planets.Terrestrial Antarctica is among the most extreme environments on Earth. Its inhabitants experience the cumulative stresses of freezing temperatures, limited carbon, nitrogen and water availability, strong UV radiation, and frequent freeze-thaw cycles 2,10,11 . Although it was once believed that these conditions restrict life, we now know that the continent hosts a surprising diversity of macrofauna and microbiota 1,2,12 . Surveys indicate that the phylum-level composition of microbial communities in Antarctic soils is similar to those of temperate soils 3 , but Antarctic communities are highly specialized at the species level and strongly structured by physicochemical factors 1,3,10 . In many Antarctic soils, microorganisms are thought to live in dormant states 2 , with metabolic energy directed towards cell maintenance rather than growth 13 . However, it is unclear how these communities obtain the energy and carbon needed for maintenance, given that these soils are often low in organic carbon and contain few classical primary producers 2,5 .

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Distinct form I, II, III, and IV Rubisco proteins from the three kingdoms of life provide clues about Rubisco evolution and structure/function relationships

Cited by 365 publications

References 40 publications

Constraining the timing of the Great Oxidation Event within the Rubisco phylogenetic tree

Constraining the timing of the Great Oxidation Event within the Rubisco phylogenetic tree

A function-based screen for seeking RubisCO active clones from metagenomes: novel enzymes influencing RubisCO activity

Atmospheric trace gases support primary production in Antarctic desert surface soil

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