Multiple Rubisco forms in proteobacteria: their functional significance in relation to CO2 acquisition by the CBB cycle

Abstract

Rubisco is the predominant enzymatic mechanism in the biosphere by which autotrophic bacteria, algae, and terrestrial plants fix CO(2) into organic biomass via the Calvin-Benson-Basham reductive pentose phosphate pathway. Rubisco is not a perfect catalyst, suffering from low turnover rates, a low affinity for its CO(2) substrate, and a competitive inhibition by O(2) as an alternative substrate. As a consequence of changing environmental conditions over the past 3.5 billion years, with decreasing CO(2) and increasing O(2) in the atmosphere, Rubisco has evolved into multiple enzymatic forms with a range of kinetic properties, as well as co-evolving with CO(2)-concentrating mechanisms to cope with the different environmental contexts in which it must operate. The most dramatic evidence of this is the occurrence of multiple forms of Rubisco within autotrophic proteobacteria, where Forms II, IC, IBc, IAc, and IAq can be found either singly or in multiple combinations within a particular bacterial genome. Over the past few years there has been increasing availability of genomic sequence data for bacteria and this has allowed us to gain more extensive insights into the functional significance of this diversification. This paper is focused on summarizing what is known about the diversity of Rubisco forms, their kinetic properties, development of bacterial CO(2)-concentrating mechanisms, and correlations with metabolic flexibility and inorganic carbon environments in which proteobacteria perform various types of obligate and facultative chemo- and photoautotrophic CO(2) fixation.

Genomic insights into the uncultivated marine Zetaproteobacteria at Loihi Seamount

“…Therefore, while both isolates encode Form I and Form II RubisCO genes, it is unlikely that all Zetaproteobacteria do. The presence of Form II rather than Form I is interesting as it is indicative of adaptations to high CO 2 and very low O 2 environments (Badger and Bek, 2008;Tabita et al, 2008), which is consistent with the O 2 profiles presented by Glazer and Rouxel (2009), in which the O 2 levels at Loihi Seamount iron mats were often below the detection limit (3 mM) even at the mat surface. These findings suggest that the broad phylogenetic spectrum of Zetaproteobacteria represented by SAGs analyzed in this study have a lower O 2 tolerance for fixing carbon compared with their cultivated counterparts.…”

Evidence for hydrogen oxidation and metabolic plasticity in widespread deep-sea sulfur-oxidizing bacteria

“…This form II RuBisCO is also present in the Saanich Inlet OMZ SUP05 (9) and the clam symbionts Candidatus Ruthia magnifica (18) and Candidatus Vesicomyosocius okutanii (21). In contrast, the H 2 -oxidizing symbionts of Bathymodiolus mussels (4) possess genes for a form I RuBisCO, which is optimized for higher O 2 and lower CO 2 concentration (32). The presence of genes in GB SUP05 encoding for form II RuBisCO enzymes typically adapted to low O 2 and high CO 2 concentrations is consistent with the low O 2 conditions of the deep GB.…”

Comparative metagenomics of microbial communities inhabiting deep-sea hydrothermal vent chimneys with contrasting chemistries

“…Upstream of cbbLS, no genes involved in the CBB cycle were identified (Figure 3). A similar cbb gene cluster with conserved cbbLSQO gene organization has been found in the chemoautotrophic Gammaproteobacteria Thiomirospira crunogena XCL-2, Hydrogenovibrio marinus and the endosymbiont of Solemya velum (Badger and Bek, 2008). It has been observed that the CBB cycle genes of obligate autotrophs apparently do not form CBB operons that would facilitate coordinated regulation, presumably because these genes are constitutively expressed and, therefore, do not require regulation in these obligate autotrophs .…”