Heterocyst envelope thickness, heterocyst frequency and nitrogenase activity in Anabaena flos-aquae: influence of exogenous oxygen tension

Kangatharalingam, N.; Priscu, John C.; Paerl, Hans W.

doi:10.1099/00221287-138-12-2673

Cited by 33 publications

(25 citation statements)

References 23 publications

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“…Importantly, this speculative link between the isotopic effect and heterocyst number is merely a hypothesis suggested by our observed data and should be further investigated. Previous studies have shown that heterocyst frequency does not directly correlate with nitrogenase activity (e.g., Kangatharalingam, Priscu, & Paerl, 1992), and we acknowledge this relationship is likely more complex than our interpretation. However, given that pN 2 exerts a clear influence on heterocyst frequency (Figure 4), we interrogate our data under the assumption that (with all other parameters equal) pN 2 affects the kinetics of nitrogenase.…”

Section: Nitrogen Isotope Fractionation In Anabaena Speciesmentioning

confidence: 49%

Morphological and isotopic changes of heterocystous cyanobacteria in response to N₂ partial pressure

et al. 2018

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Earth's atmospheric composition has changed significantly over geologic time. Many redox active atmospheric constituents have left evidence of their presence, while inert constituents such as dinitrogen gas (N2) are more elusive. In this study, we examine two potential biological indicators of atmospheric N2: the morphological and isotopic signatures of heterocystous cyanobacteria. Biological nitrogen fixation constitutes the primary source of fixed nitrogen to the global biosphere and is catalyzed by the oxygen‐sensitive enzyme nitrogenase. To protect this enzyme, some filamentous cyanobacteria restrict nitrogen fixation to microoxic cells (heterocysts) while carrying out oxygenic photosynthesis in vegetative cells. Heterocysts terminally differentiate in a pattern that is maintained as the filaments grow, and nitrogen fixation imparts a measurable isotope effect, creating two biosignatures that have previously been interrogated under modern N2 partial pressure (pN2) conditions. Here, we examine the effect of variable pN2 on these biosignatures for two species of the filamentous cyanobacterium Anabaena. We provide the first in vivo estimate of the intrinsic isotope fractionation factor of Mo‐nitrogenase (εfix = −2.71 ± 0.09‰) and show that, with decreasing pN2, the net nitrogen isotope fractionation decreases for both species, while the heterocyst spacing decreases for Anabaena cylindrica and remains unchanged for Anabaena variabilis. These results are consistent with the nitrogen fixation mechanisms available in the two species. Application of these quantifiable effects to the geologic record may lead to new paleobarometric measurements for pN2, ultimately contributing to a better understanding of Earth's atmospheric evolution.

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Section: Nitrogen Isotope Fractionation In Anabaena Speciesmentioning

confidence: 49%

Morphological and isotopic changes of heterocystous cyanobacteria in response to N₂ partial pressure

et al. 2018

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“…An apparent increase in the average thickness of the glycolipid layer in DR1822 relative to that in the wild-type strain (Fig. 4) may be a response to penetration of oxygen (23).…”

Section: Resultsmentioning

confidence: 99%

Lipopolysaccharide dependence of cyanophage sensitivity and aerobic nitrogen fixation in Anabaena sp. strain PCC 7120

Khudyakov

Wölk

1997

J Bacteriol

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FoxLipopolysaccharide (LPS) is a major component of the outer membrane of gram-negative bacteria. The diverse O antigen portion is an important determinant of the surface character of the cells, including their outer membrane permeability (38), electrical charge (44), reactivity to antibodies, and susceptibility to phages (32), and so affects the adaptation of bacteria to their environments. LPSs of many bacteria also show potent endotoxin activity (22). In cyanobacteria, LPS may adsorb cyanophage (42), and its endotoxin activity may affect aquatic habitats (25).LPS consists of three covalently linked domains: lipid A, oligosaccharide core, and O antigen. The O antigen portion is comprised of serially repeated, strain-specific oligosaccharide units. This polymer of oligosaccharide units is the immunodominant portion of the LPS and often serves as a bacteriophage receptor. Assembly of the lipid A-core portion and synthesis of the O antigen units are directed by the rfa and rfb genes, respectively. In a "block" mechanism of O antigen synthesis, repeating subunits of the O antigen, synthesized by sequential transfer of monosaccharide constituents to a lipid carrier at the cytosolic side of the cytoplasmic membrane, are transported to the periplasmic side of the cell membrane and polymerized. The polymerization, directed by rfc genes, entails transfer of an already synthesized unit or polymer of units to the reducing terminus of a single lipid-linked unit (34,45). Assembly of LPS is completed by ligation of an entire polysaccharide chain to oligosaccharide core-lipid A. Finally, LPS is translocated to the outer membrane. All of the enzymes, lipid carriers, intermediates, and LPS itself are membrane bound. In this mechanism for LPS synthesis, the first monosaccharide residue transferred to a lipid carrier is galactose-1-phosphate. The gene, rfbP, responsible for the transfer of that galactosyl residue is indicative of the block mechanism of LPS synthesis. An alternative, monomeric mechanism of O antigen synthesis proceeds at the cytoplasmic membrane by sequential addition of mannosyl residues to the nonreducing terminus of the forming chain and leads to the synthesis of an LPS in which the repeating subunit of O antigen contains three or five interlinked mannosyl residues (22,45).Cyanobacteria are a group of oxygenic, photosynthetic gram-negative bacteria. Although the wall of cyanobacterial vegetative cells has been incompletely defined, chemically, LPS is typically a constituent and contains domains that are similar to those in other bacteria (14). The LPS of the unicellular species Anacystis nidulans KM has been studied in detail (24). Its O antigen, reminiscent of the O antigen of Escherichia coli O8 and O9, contains 1,4-interlinked trisaccharides of 1,3-linked mannosyl residues. As in other phototrophic bacteria, some of the mannosyl residues are methylated. The O antigen of a filamentous species, Anabaena variabilis, contains L-acofriose, L-rhamnose, D-mannose, D-glucose, and D-galactose (50), suggestive of a b...

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“…Under the controlled conditions in which isolated strains are grown, the need for different HG types may not be as high as in natural environments, thus resulting in more simple HG profiles. In this sense, Kangatharalingam et al (1992), for example, demonstrated that heterocyst glycolipid-layer thickness was dependent on exogenous oxygen tension. Whether such thickening could imply changes in the HG composition remains unknown.…”

Section: Environmental Factors Influencing Hg Distribution-mentioning

confidence: 99%

Cyanobacterial heterocyst glycolipids in cultures and environmental samples: Diversity and biomarker potential

Wörmer¹,

Cirés²,

Velázquez³

et al. 2012

Limnology & Oceanography

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The envelope of cyanobacterial heterocysts contains characteristic glycolipids termed heterocyst glycolipids (HGs). Six cultures of heterocyst-forming cyanobacteria, as well as samples from 2 polar ecosystems and 12 Spanish freshwaters, were analyzed for their HG content. We tentatively identified four novel HGs in the cyanobacterial strains, including derivatives with a nonhexose sugar moiety. We observed unexpectedly diverse HG distributions in cultures, with very singular fingerprinting for Aphanizomenon aphanizomenoides and Aphanizomenon ovalisporum, thus supporting the taxonomic robustness of HGs. The analysis of HGs in environmental samples revealed even larger diversity and increased abundance of certain HGs that are minor components in cultured strains. Interpretation of HG patterns could be applied to support taxonomic characterization of the community of heterocystous cyanobacteria and to detect changes in the cyanobacterial consortia mediating N 2 fixation. In addition to taxonomy, environmental factors seem to influence the biosynthesis of HGs. For example, in our studied environmental samples, temperature appears to influence the relative distribution of keto-hexacosanol and hexacosanediols, as previously proposed for cultures. Our results extend the knowledge of HG distributions in cyanobacteria and the environment and illustrate the potential of HGs as biomarkers for applications in both ecological and paleoenvironmental studies.

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Heterocyst envelope thickness, heterocyst frequency and nitrogenase activity in Anabaena flos-aquae: influence of exogenous oxygen tension

Cited by 33 publications

References 23 publications

Morphological and isotopic changes of heterocystous cyanobacteria in response to N₂ partial pressure

Morphological and isotopic changes of heterocystous cyanobacteria in response to N₂ partial pressure

Lipopolysaccharide dependence of cyanophage sensitivity and aerobic nitrogen fixation in Anabaena sp. strain PCC 7120

Cyanobacterial heterocyst glycolipids in cultures and environmental samples: Diversity and biomarker potential

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Heterocyst envelope thickness, heterocyst frequency and nitrogenase activity in Anabaena flos-aquae: influence of exogenous oxygen tension

Cited by 33 publications

References 23 publications

Morphological and isotopic changes of heterocystous cyanobacteria in response to N2 partial pressure

Morphological and isotopic changes of heterocystous cyanobacteria in response to N2 partial pressure

Lipopolysaccharide dependence of cyanophage sensitivity and aerobic nitrogen fixation in Anabaena sp. strain PCC 7120

Cyanobacterial heterocyst glycolipids in cultures and environmental samples: Diversity and biomarker potential

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Morphological and isotopic changes of heterocystous cyanobacteria in response to N₂ partial pressure

Morphological and isotopic changes of heterocystous cyanobacteria in response to N₂ partial pressure