A non-carboxylating pentose bisphosphate pathway in halophilic archaea

Abstract

Bacteria and Eucarya utilize the non-oxidative pentose phosphate pathway to direct the ribose moieties of nucleosides to central carbon metabolism. Many archaea do not possess this pathway, and instead, Thermococcales utilize a pentose bisphosphate pathway involving ribose-1,5-bisphosphate (R15P) isomerase and ribulose-1,5-bisphosphate (RuBP) carboxylase/oxygenase (Rubisco). Intriguingly, multiple genomes from halophilic archaea seem only to harbor R15P isomerase, and do not harbor Rubisco. In this study, we identify a previously unrecognized nucleoside degradation pathway in halophilic archaea, composed of guanosine phosphorylase, ATP-dependent ribose-1-phosphate kinase, R15P isomerase, RuBP phosphatase, ribulose-1-phosphate aldolase, and glycolaldehyde reductase. The pathway converts the ribose moiety of guanosine to dihydroxyacetone phosphate and ethylene glycol. Although the metabolic route from guanosine to RuBP via R15P is similar to that of the pentose bisphosphate pathway in Thermococcales, the downstream route does not utilize Rubisco and is unique to halophilic archaea.

Discovery of the Streamlined Haloarchaeon Halorutilus salinus , Comprising a New Order Widespread in Hypersaline Environments across the World

“…Asgardarchaeota, the methanogenic Methanonatronarchaeia , the hyperthermophilic archaeon Thermococcus kodakarensis, and the DPANN superphylum [ 66 – 69 ]). Although several halophilic archaea encode ribose 1,5-biphosphate isomerase ( 64 ), the evidence of type III-like RuBisCO presence has been only recently reported in members of this group ( 70 ); making strain F3-133 T one of the first known examples. Unexpectedly, strain F3-133 T ’s type III RuBisCO exhibited higher similarities to sequences from the archaeal phyla Candidatus Nanohaloarchaea or Division MSBL-1, than to Halobacteria class representatives.…”

Utilizing Ribose 1,5-Bisphosphate Isomerase and RuBisCO-Equipped Escherichia coli Nissle for Low-Carbon Footprint GABA Production

“…Escherichia coli Nissle (EcN) is the only representative probiotic from E. coli lineages and has been marketed under the Mutaflor trademark as an intestinal resistance for almost a century . EcN possesses an acidophilic nature and substantial gene mutations compared to commensal E. coli K-12 and B strains. − Recently, exploration of EcN usage has been broadened for a safe endo- and exochemical producer, such as heparosan, p -coumaric acid, β-alanine, butyric acid, and γ-aminobutyrate (GABA). − Nonetheless, deleterious CO 2 emission would be generated during chemical biosynthesis as a side-product of either metabolism or the biochemical reaction . Hence, incorporating microbial cell factories with a CO 2 -fixing system is crucial to enhancing their role in sustainability.…”

“…The Calvin-Benson-Bassham (CBB) cycle is a widely known natural CO 2 assimilation pathway among eukaryotes and prokaryotes with ribulose-1,5-bisphosphate carboxylase-oxygenase (RuBisCO, rbcLS) and phosphoribulokinase (prk) as the key enzymes. 10,11 This pathway has an interconnection with the pentose phosphate (PP) pathway as a bypass shunt from ribose 5-phosphate (Ru5P) to pentose to 3-phosphoglycerate (3PG). The PP pathway of E. coli is different from other CO 2 -fixing organisms which redirects the flux from the decomposed hexose to glyceraldehyde-3-phosphate (GAP) and fructose-6-phosphate (F6P).…”

“…R15P isomerase (R15Pi) from the 5′ adenosine monophosphate (AMP) pathway could convert R15P into ribulose 1,5-bisphosphate (RuBP), a precursor of RuBisCO, which in turn facilitated the conversion to 3PG. 11 This pathway represents a promising alternative CO 2 -fixing route within ribulose-related pathways that requires further exploration. Of high-value compounds from the decarboxylation process, GABA is a well-known inhibitory neurotransmitter drug and a fine chemical with diverse applications.…”

Non-native Pathway Engineering with CRISPRi for Carbon Dioxide Assimilation and Valued 5-Aminolevulinic Acid Synthesis in Escherichia coli Nissle

“…The common CO 2 fixation route from Ru5P into 3PG was directed using PRK and RuBisCO from Synechococcus elongatus PCC6301 (denoted as PR). 26 Another novel route between R15P and 3PG was bridged by synergizing R15P isomerase (R15PI) from Thermococcus kodakarensis ( 27 ) and RuBisCO from S. elongatus PCC6301 (denoted as RR). Subsequently, the function and efficiency of both CO 2 -fixing systems were evaluated for assimilating the release of CO 2 during 5-ALA production.…”