Phylogenetic and evolutionary relationships of RubisCO and the RubisCO-like proteins and the functional lessons provided by diverse molecular forms

Abstract

Ribulose 1,5-bisphosphate (RuBP) carboxylase/oxygenase (RubisCO) catalyses the key reaction by which inorganic carbon may be assimilated into organic carbon. Phylogenetic analyses indicate that there are three classes of bona fide RubisCO proteins, forms I, II and III, which all catalyse the same reactions. In addition, there exists another form of RubisCO, form IV, which does not catalyse RuBP carboxylation or oxygenation. Form IV is actually a homologue of RubisCO and is called the RubisCO-like protein (RLP). Both RubisCO and RLP appear to have evolved from an ancestor protein in a methanogenic archaeon, and comprehensive analyses indicate that the different forms (I, II, III and IV ) contain various subgroups, with individual sequences derived from representatives of all three kingdoms of life. The diversity of RubisCO molecules, many of which function in distinct milieus, has provided convenient model systems to study the ways in which the active site of this protein has evolved to accommodate necessary molecular adaptations. Such studies have proven useful to help provide a framework for understanding the molecular basis for many important aspects of RubisCO catalysis, including the elucidation of factors or functional groups that impinge on RubisCO carbon dioxide/oxygen substrate discrimination.

In Vivo Studies in Rhodospirillum rubrum Indicate That Ribulose-1,5-bisphosphate Carboxylase/Oxygenase (Rubisco) Catalyzes Two Obligatorily Required and Physiologically Significant Reactions for Distinct Carbon and Sulfur Metabolic Pathways

“…This is consistent with the observation that plasmids expressing Rubisco forms I and II from R. sphaeroides supported MTA-dependent photoheterotrophic growth of strain IR (⌬cbbM/ ⌬rlpA). Furthermore, the form III Rubisco (rbcL) gene from the methanogenic archaeon, M. burtonii (7,30), also complemented strain IR with MTA as sole sulfur source (Fig. 4C).…”

“…Some 17 years ago, a new member of the Rubisco family was discovered, the Rubisco-like protein (RLP), or form IV Rubisco (5). RLPs lack the capacity to catalyze the typical carboxylation reaction and have been identified in proteobacteria, cyanobacteria, archaea, and algae (6,7). No functional similarity was initially found between Rubisco and RLP due to the substitution of several key active site residues in the latter (7); indeed in Rhodospirillum rubrum, 7 of the 19 required active site residues of its form II Rubisco are altered in the R. rubrum RLP.…”

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

“…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).…”

Algal evolution in relation to atmospheric CO 2 : carboxylases, carbon-concentrating mechanisms and carbon oxidation cycles

“…The Rubisco gene family not only contains the forms I, II and III Rubiscos that catalyse the Rubisco carboxylase and Rubisco oxygenase reactions, but also the form IV Rubisco-like protein (RLP) which does not catalyse the typical Rubisco reactions and which is involved in methionine salvage in some bacteria [47][48][49]. Molecular phylogenetic analysis [47][48][49] suggests that an ancestral form III Rubisco arose in a methanogen (i.e. a member of the Archaea) and gave rise, by two vertical transmissions, to all other form III Rubiscos and to form IV.…”