Multiple Roles of Soluble Sugars in the Establishment of <i>Gunnera</i>-<i>Nostoc</i> Endosymbiosis

Khamar, Hima J.; Breathwaite, Erick; Prasse, Christine E.; Fraley, Elizabeth R.; Secor, Craig R.; Chibane, Fairouz L.; Elhai, Jeff; Chiu, Wan-Ling

doi:10.1104/pp.110.162529

Cited by 39 publications

(43 citation statements)

References 31 publications

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“…In another study, nitrogen-deprived Gunnera manicata plants were found to accumulate high levels of Glc and Fru. However, N. punctiforme colonization drastically reduced the levels of these sugars at the colonization sites in the plant (Khamar et al, 2010). Our results do not rule out the possibility that Fru or any other sugar that can be assimilated by N. punctiforme, such as Suc or Rib, has a role in nutrition of the cyanobacterial symbiont.…”

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confidence: 76%

“…The cyanobacterium in the symbiosis has a low photosynthetic activity and in turn is supplemented by the plant partner with sugars (Adams and Duggan, 2008;Meeks, 2009). Although Fru and Glc have been suggested to be the sugars supplied by some plant partners (Wouters et al, 2000;Khamar et al, 2010), exactly which sugars and cyanobacterial sugar uptake mechanism(s) are involved in the symbiosis is unknown.…”

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confidence: 99%

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A Nostoc punctiforme Sugar Transporter Necessary to Establish a Cyanobacterium-Plant Symbiosis

et al. 2013

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In cyanobacteria-plant symbioses, the symbiotic nitrogen-fixing cyanobacterium has low photosynthetic activity and is supplemented by sugars provided by the plant partner. Which sugars and cyanobacterial sugar uptake mechanism(s) are involved in the symbiosis, however, is unknown. Mutants of the symbiotically competent, facultatively heterotrophic cyanobacterium Nostoc punctiforme were constructed bearing a neomycin resistance gene cassette replacing genes in a putative sugar transport gene cluster. Results of transport activity assays using 14 C-labeled fructose and glucose and tests of heterotrophic growth with these sugars enabled the identification of an ATP-binding cassette-type transporter for fructose (Frt), a major facilitator permease for glucose (GlcP), and a porin needed for the optimal uptake of both fructose and glucose. Analysis of green fluorescent protein fluorescence in strains of N. punctiforme bearing frt::gfp fusions showed high expression in vegetative cells and akinetes, variable expression in hormogonia, and no expression in heterocysts. The symbiotic efficiency of N. punctiforme sugar transport mutants was investigated by testing their ability to infect a nonvascular plant partner, the hornwort Anthoceros punctatus. Strains that were specifically unable to transport glucose did not infect the plant. These results imply a role for GlcP in establishing symbiosis under the conditions used in this work.

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confidence: 76%

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confidence: 99%

A Nostoc punctiforme Sugar Transporter Necessary to Establish a Cyanobacterium-Plant Symbiosis

et al. 2013

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“…S4. N. punctiforme strain UCD 153 and its derivatives were cultured in Allan and Arnon medium diluted fourfold (AA/4), as described previously (21), with the exception that cultures were supplemented with 30 mM fructose to suppress hormogonium differentiation (22). For nitrogen step-down, cultures supplemented with 2.5 mM NH 4 Cl at a chlorophyll (Chl) a concentration of 2-3 μg/mL were harvested at 1,000 × g for 5 min, washed three times with AA/4, and suspended in AA/4 (21).…”

Section: Methodsmentioning

confidence: 99%

Biased inheritance of the protein PatN frees vegetative cells to initiate patterned heterocyst differentiation

Risser

Wong

Meeks

2012

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

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Heterocysts, cells specialized for nitrogen fixation in certain filamentous cyanobacteria, appear singly in a nonrandom spacing pattern along the chain of vegetative cells. A two-stage, biased initiation and competitive resolution model has been proposed to explain the establishment of this spacing pattern. There is substantial evidence that competitive resolution of a subset of cells initiating differentiation occurs by interactions between a selfenhancing activator protein, HetR, and a diffusible pentapeptide inhibitor PatS-5 (RGSGR). Results presented here show that the absence of a unique membrane protein, PatN, in Nostoc punctiforme strain ATCC 29133 leads to a threefold increase in heterocyst frequency and a fourfold decrease in the vegetative cell interval between heterocysts. A PatN-GFP translational fusion shows a pattern of biased inheritance in daughter vegetative cells of ammonium-grown cultures. Inactivation of another heterocyst patterning gene, patA, is epistatic to inactivation of patN, and transcription of patA increases in a patN-deletion strain, implying that patN may function by modulating levels of patA. The presence of PatN is hypothesized to decrease the competency of a vegetative cell to initiate heterocyst differentiation, and the cellular concentration of PatN is dependent on cell division that results in cells transiently depleted of PatN. We suggest that biased inheritance of cell-fate determinants is a phylogenetic domain-spanning paradigm in the development of biological patterns.activator-inhibitor | pattern differentiation T wo broad strategies used in the development of biological patterns are activator-inhibitor systems, a refinement of Turing-type reaction-diffusion systems (1, 2), and differential inheritance of cell fate determinants (3, 4). These strategies have been analyzed in multicellular eukaryotes ranging in developmental complexity from hydra to vertebrates (1, 4). Some filamentous cyanobacteria show spaced patterns of differentiated cells, such as nitrogen-fixing heterocysts and spore-like akinetes, thereby representing the simplest and oldest evolutionary model for study of the development of biological patterns and multicellular interactions. There is strong experimental evidence that an activatorinhibitor system regulates heterocyst patterning in filamentous cyanobacteria (5-7). We report here the characteristics of a gene (patN) that is required for normal heterocyst patterning, and the phenotype and protein localization of which is consistent with a role in the biased initiation of heterocyst differentiation via biased inheritance.Heterocysts terminally differentiate from vegetative cells in response to limitation of combined nitrogen. The heterocysts appear in a nonrandom spacing of approximately 1 heterocyst to every 10-15 vegetative cells. The activator-inhibitor system governing this patterning consists of a self-enhancing activator protein, HetR (8, 9), and its antagonist, proteins containing a pentapeptide, PatS-5 (RGSGR) (10, 11). These two primary positi...

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“…This factor induces hpnP expression in response to osmotic stress in R. palustris (Kulkarni et al, 2013); osmolyte production by plants in the rhizosphere is well documented, and in some cases has been shown to promote plant-microbe symbioses (Miller and Wood, 1996;Khamar et al, 2010).…”

Section: -Mebhp Production Is Niche Specific Jn Ricci Et Almentioning

confidence: 99%

Diverse capacity for 2-methylhopanoid production correlates with a specific ecological niche

et al. 2013

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Molecular fossils of 2-methylhopanoids are prominent biomarkers in modern and ancient sediments that have been used as proxies for cyanobacteria and their main metabolism, oxygenic photosynthesis. However, substantial culture and genomic-based evidence now indicates that organisms other than cyanobacteria can make 2-methylhopanoids. Because few data directly address which organisms produce 2-methylhopanoids in the environment, we used metagenomic and clone library methods to determine the environmental diversity of hpnP, the gene encoding the C-2 hopanoid methylase. Here we show that hpnP copies from alphaproteobacteria and as yet uncultured organisms are found in diverse modern environments, including some modern habitats representative of those preserved in the rock record. In contrast, cyanobacterial hpnP genes are rarer and tend to be localized to specific habitats. To move beyond understanding the taxonomic distribution of environmental 2-methylhopanoid producers, we asked whether hpnP presence might track with particular variables. We found hpnP to be significantly correlated with organisms, metabolisms and environments known to support plant-microbe interactions (P-valueo10 À 6 ); in addition, we observed diverse hpnP types in closely packed microbial communities from other environments, including stromatolites, hot springs and hypersaline microbial mats. The common features of these niches indicate that 2-methylhopanoids are enriched in sessile microbial communities inhabiting environments low in oxygen and fixed nitrogen with high osmolarity. Our results support the earlier conclusion that 2-methylhopanoids are not reliable biomarkers for cyanobacteria or any other taxonomic group, and raise the new hypothesis that, instead, they are indicators of a specific environmental niche.

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Multiple Roles of Soluble Sugars in the Establishment of Gunnera-Nostoc Endosymbiosis

Cited by 39 publications

References 31 publications

A Nostoc punctiforme Sugar Transporter Necessary to Establish a Cyanobacterium-Plant Symbiosis

A Nostoc punctiforme Sugar Transporter Necessary to Establish a Cyanobacterium-Plant Symbiosis

Biased inheritance of the protein PatN frees vegetative cells to initiate patterned heterocyst differentiation

Diverse capacity for 2-methylhopanoid production correlates with a specific ecological niche

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