Carotenoids of Gemmatimonas aurantiaca (Gemmatimonadetes): identification of a novel carotenoid, deoxyoscillol 2-rhamnoside, and proposed biosynthetic pathway of oscillol 2,2′-dirhamnoside

Abstract

Gemmatimonas aurantiaca strain T-27 T is an orange-coloured, Gram-negative, facultatively aerobic, polyphosphate-accumulating bacterium belonging to a recently proposed phylum, Gemmatimonadetes. We purified its pigments and identified them as carotenoids and their glycoside derivatives using spectral data. The major carotenoid was (2S,29S)-oscillol 2,29-di-(a-Lrhamnoside), and the minor carotenoids were (2S)-deoxyoscillol 2-(a-L-rhamnoside) and didemethylspirilloxanthin. Deoxyoscillol 2-rhamnoside is a novel carotenoid. Oscillol 2,29-diglycosides have hitherto only been reported in a limited number of cyanobacteria, and this is believed to be the first finding of such carotenoids in another bacterial phylum. Based on the identification of the carotenoids and the completion of the entire nucleotide sequence, we propose a biosynthetic pathway for the carotenoids and the corresponding genes and enzymes. We propose the involvement of geranylgeranyl pyrophosphate synthase (CrtE), phytoene synthase (CrtB) and phytoene desaturase (CrtI) for lycopene synthesis; and of carotenoid 1,2-hydratase (CruF) and carotenoid 2-O-rhamnosyltransferase (CruG) for oscillol 2,29-dirhamnoside synthesis. Further, isopentenyl pyrophosphate could be synthesized by a non-mevalonate pathway (DXP pathway).

Functional type 2 photosynthetic reaction centers found in the rare bacterial phylum Gemmatimonadetes

“…In line with the presence of these carotenoids, we have identified six carotenogenesis genes in the AP64 genome (SI Appendix, Table S6) and propose a putative biosynthesis pathway for spirilloxanthin and oscillol series carotenoid biosynthesis (SI Appendix, Fig. S4), based on available genetic information and previously reported data (29,30).…”

“…In addition, AP64 contains several main carotenoids, mostly various derivatives of spirilloxanthin and oscillol (29) (Fig. 3C).…”

Nitrous Oxide Reduction by an Obligate Aerobic Bacterium, Gemmatimonas aurantiaca Strain T-27

“…Apart from the synthesis of a novel carotenoid by G. aurantiaca strain T-27 (31), not much has been reported regarding their physiology until recently, mainly due to the paucity of available isolates. The recent discovery of a full operon encoding type 2 photosynthetic reaction centers in the G. phototrophica strain AP-64 genome suggested that the Gemmatimonadetes phylum of bacteria may have adopted an oxygen-independent energy-generating metabolism to supplement an oxygen-dependent heterotrophic lifestyle in cases of transient hypoxia or anoxia (32).…”

Gemmatirosa kalamazoonesis gen. nov., sp. nov., a member of the rarely-cultivated bacterial phylum Gemmatimonadetes

“…S2). G. aurantiaca T-27 produced orange-colored carotenoids which are thought to act as a defense mechanism against oxygen radicals (Takaichi et al, 2010); it is hypothesized that the pink pigment produced by KBS708 may serve a similar function, contributing to KBS708 s oxygen tolerance. Microscopic imagery confirmed the presence of extracellular polymers causing cells to stick together (Fig.…”