Diversity of Photosynthetic Bradyrhizobium Strains from Stem Nodules of Aeschynomene Species

Lorquin, Jean; Molouba, Flore; Dupuy, Nicolas; Ndiaye, Saliou; Alazard, Didier; Gillis, Monique; Dreyfus, B

doi:10.1007/978-94-017-2416-6_57

Cited by 20 publications

(14 citation statements)

References 8 publications

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“…In Bradyrhizobium sp. strain ORS278, canthaxanthin production is stimulated by light (13), suggesting that the expression of canthaxanthin biosynthesis genes is regulated by photoinduction, as already reported for other pigments in different organisms (2, 7). Production of this pigment could be optimized by identifying the signal transduction system controlling canthaxanthin biosynthesis.…”

Section: Figsupporting

confidence: 75%

Isolation and Characterization of Canthaxanthin Biosynthesis Genes from the Photosynthetic Bacterium Bradyrhizobium sp. Strain ORS278

et al. 2000

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A carotenoid biosynthesis gene cluster involved in canthaxanthin production was isolated from the photosynthetic Bradyrhizobium sp. strain ORS278. This cluster includes five genes identified as crtE, crtY, crtI, crtB, and crtW that are organized in at least two operons. The functional assignment of each open reading frame was confirmed by complementation studies.Bradyrhizobium strains isolated from Aeschynomene stem nodules are photosynthetic (4; see reference 6 for a review), which is a rare trait in Rhizobium bacteria. These strains exhibit a photoheterotrophic and strictly aerobic photosynthesis (6; A. Vermeglio, personal communication). In culture, most of these stem isolates show the same pink coloration, while a few strains produce orange pigmentation (12, 16). Pigment analyses showed that bacteriochlorophyll and spirilloxanthin, two pigments of the light harvesting system, are common to all of these photosynthetic Bradyrhizobium strains, whereas orange strains produce an additional bicyclic carotenoid, canthaxanthin (4,4Ј-diketo-␤-carotene) (12). This was the first report on the presence of this carotenoid in photosynthetic bacteria. Bradyrhizobium sp. strain ORS278 produces the highest quantity of canthaxanthin of all tested photosynthetic bacteria; canthaxanthin represents 85% of its total carotenoid content (12).Contrary to anaerobic purple phototrophic bacteria, aerobic phototrophic bacteria synthesize an unusually diverse variety of carotenoids, including photosynthetic carotenoids such as spirilloxanthin or spheroidenone, and often a large amount of bicyclic carotenoid (␤-carotene and hydroxyl derivatives) (24; see reference 26 for a review). These carotenoids were shown to not be bound to the photosynthetic apparatus of these aerobic bacteria (17,27) and their function is still unclear-

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Section: Figsupporting

confidence: 75%

Isolation and Characterization of Canthaxanthin Biosynthesis Genes from the Photosynthetic Bacterium Bradyrhizobium sp. Strain ORS278

et al. 2000

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“…This observation is rather puzzling considering that in nature, mainly photosynthetic Bradyrhizobium strains, lacking a T3SS, were isolated from root and stem nodules of NF-independent Aeschynomene species (Lorquin et al, 1993;Molouba et al, 1999;Montecchia et al, 2002). Nevertheless, one study reported the isolation of a few non-photosynthetic Bradyrhizobium strains isolated from A. indica species growing in French Guiana (Miché et al, 2010).…”

Section: Discussionmentioning

confidence: 99%

Rhizobium–legume symbiosis in the absence of Nod factors: two possible scenarios with or without the T3SS

et al. 2015

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The occurrence of alternative Nod factor (NF)-independent symbiosis between legumes and rhizobia was first demonstrated in some Aeschynomene species that are nodulated by photosynthetic bradyrhizobia lacking the canonical nodABC genes. In this study, we revealed that a large diversity of non-photosynthetic bradyrhizobia, including B. elkanii, was also able to induce nodules on the NFindependent Aeschynomene species, A. indica. Using cytological analysis of the nodules and the nitrogenase enzyme activity as markers, a gradient in the symbiotic interaction between bradyrhizobial strains and A. indica could be distinguished. This ranged from strains that induced nodules that were only infected intercellularly to rhizobial strains that formed nodules in which the host cells were invaded intracellularly and that displayed a weak nitrogenase activity. In all nonphotosynthetic bradyrhizobia, the type III secretion system (T3SS) appears required to trigger nodule organogenesis. In contrast, genome sequence analysis revealed that apart from a few exceptions, like the Bradyrhizobium ORS285 strain, photosynthetic bradyrhizobia strains lack a T3SS. Furthermore, analysis of the symbiotic properties of an ORS285 T3SS mutant revealed that the T3SS could have a positive or negative role for the interaction with NF-dependent Aeschynomene species, but that it is dispensable for the interaction with all NF-independent Aeschynomene species tested. Taken together, these data indicate that two NF-independent symbiotic processes are possible between legumes and rhizobia: one dependent on a T3SS and one using a so far unknown mechanism.

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“…Bradyrhizobium sp. strain ORS278 (12), called the wild-type strain throughout this study, and isogenic mutants 278⌬pufLM and 278⌬hmuO constructed in this work were grown in a modified YM medium (pH 6.8) containing (per liter) 2.5 g of sodium glutamate, 2 g of yeast extract, 0.66 g of K 2 HPO 4 , 0.05 g of NaCl, 0.1 g of MgSO 4 ⅐7H 2 O, 0.04 g of CaCl 2 , and 0.004 g of FeCl 3 . Strains were grown aerobically in a gyratory shaker (170 rpm) at 37°C in either complete darkness or continuous white light with a bank of incandescent bulbs or under a light͞dark cycle (16 h͞8 h).…”

Section: Methodsmentioning

confidence: 99%

Effect of Bradyrhizobium photosynthesis on stem nodulation of Aeschynomene sensitiva

Giraud

Hannibal

Fardoux

et al. 2000

Proc. Natl. Acad. Sci. U.S.A.

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Some leguminous species of the genus Aeschynomene are specifically stem-nodulated by photosynthetic bradyrhizobia. To study the effect of bacterial photosynthesis during symbiosis, we generated a photosynthesis-negative mutant of the Bradyrhizobium sp. strain ORS278 symbiont of Aeschynomene sensitiva. The presence of a functional photosynthetic unit in bacteroids and the high expression of the photosynthetic genes observed in stem nodules demonstrate that the bacteria are photosynthetically active during stem symbiosis. Stem inoculation by the photosynthetic mutant gave a 50% decrease in stem-nodule number, which reduced nitrogen fixation activity and plant growth in the same proportion. These results indicate an important role of bacterial photosynthesis in the efficiency of stem nodulation.R hizobia interact symbiotically with leguminous plants by inducing nitrogen-fixing nodules on the roots. Some plants of the genus Aeschynomene, encountered in waterlogged soils or riverbanks, have the peculiar property of forming stem nodules. This very unusual behavior among leguminous plants is shared only with a few species of the genera Sesbania, Neptunia, and Discolobium (1). Rhizobia isolated from Aeschynomene stem nodules exhibit a property uncommon among other rhizobia of developing a photosynthetic system (2, 3). This was first demonstrated in the case of a strain isolated from Aeschynomene indica stem nodules and designated BTAi 1 (2). In ex planta culture, BTAi 1 required a photoperiod for production and accumulation of bacteriochlorophyll a and exhibited a photoheterotrophic and strictly aerobic photosynthesis (4, 5). In this respect, the photosynthetic activity of the bacteriochlorophyll-containing rhizobia most closely resembles that of the aerobic anoxygenic photosynthetic bacteria (6, 7).Since the discovery of BTAi 1, several other rhizobia isolated from Aeschynomene stem nodules have been reported to produce bacteriochlorophyll a (8 -13). These photosynthetic Aeschynomene rhizobia were shown to form a separate subbranch of the Bradyrhizobium rRNA lineage, distinct from Bradyrhizobium japonicum and Bradyrhizobium elkanii (13). All photosynthetic strains were shown to nodulate stem-nodulating Aeschynomene species specifically (13), indicating that the photosynthetic character of these rhizobia could play an important role during this unusual symbiosis. The demonstration by Evans et al. (4) that illumination of the stem nodules of A. indica by far-red light consistently accelerated acetylene reduction and the report of Fleischman and Kramer (3) on the presence of bacteriochlorophyll a in bacteroids isolated from stem nodules of Aeschynomene aspera provide further evidence for the importance of the photochemical activity of the endophytes in the stem nodules. However, no genetic study has determined the real contribution of the bacterial photosynthesis in the symbiotic interaction and its impact on plant growth.In purple bacteria, most of the genes required for the formation of the photosystem are clustered in...

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Diversity of Photosynthetic Bradyrhizobium Strains from Stem Nodules of Aeschynomene Species

Cited by 20 publications

References 8 publications

Isolation and Characterization of Canthaxanthin Biosynthesis Genes from the Photosynthetic Bacterium Bradyrhizobium sp. Strain ORS278

Isolation and Characterization of Canthaxanthin Biosynthesis Genes from the Photosynthetic Bacterium Bradyrhizobium sp. Strain ORS278

Rhizobium–legume symbiosis in the absence of Nod factors: two possible scenarios with or without the T3SS

Effect of Bradyrhizobium photosynthesis on stem nodulation of Aeschynomene sensitiva

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