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Mechanical regulation of photosynthesis in cyanobacteria

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Kristin A. Moore
Kristin A. Moore
Kristin A. Moore
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Sabina Altus at Pacific Northwest National Laboratory
Sabina Altus
Jian W. Tay
Jian W. Tay
Jian W. Tay
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Janet B. Meehl
Janet B. Meehl
Janet B. Meehl
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Abstract and Figures

Photosynthetic organisms regulate their responses to many diverse stimuli in an effort to balance light harvesting with utilizable light energy for carbon fixation and growth (source–sink regulation). This balance is critical to prevent the formation of reactive oxygen species that can lead to cell death. However, investigating the molecular mechanisms that underlie the regulation of photosynthesis in cyanobacteria using ensemble-based measurements remains a challenge due to population heterogeneity. Here, to address this problem, we used long-term quantitative time-lapse fluorescence microscopy, transmission electron microscopy, mathematical modelling and genetic manipulation to visualize and analyse the growth and subcellular dynamics of individual wild-type and mutant cyanobacterial cells over multiple generations. We reveal that mechanical confinement of actively growing Synechococcus sp. PCC 7002 cells leads to the physical disassociation of phycobilisomes and energetic decoupling from the photosynthetic reaction centres. We suggest that the mechanical regulation of photosynthesis is a critical failsafe that prevents cell expansion when light and nutrients are plentiful, but when space is limiting. These results imply that cyanobacteria must convert a fraction of the available light energy into mechanical energy to overcome frictional forces in the environment, providing insight into the regulation of photosynthesis and how microorganisms navigate their physical environment.
Representative cell number and endogenous fluorescence traces Each panel represents number of cells (black) and mean endogenous fluorescence intensity (emission Cy5 705/72 nm following 640 nm excitation) of all cells (blue) during microcolony formation. Data is from four individual microcolonies, which started with either one or two cells. The red arrow indicates the beginning of fluorescence rise at the 4-cell colony stage.
Representative cell number and endogenous fluorescence traces Each panel represents number of cells (black) and mean endogenous fluorescence intensity (emission Cy5 705/72 nm following 640 nm excitation) of all cells (blue) during microcolony formation. Data is from four individual microcolonies, which started with either one or two cells. The red arrow indicates the beginning of fluorescence rise at the 4-cell colony stage.
… 
Transmission electron micrographs of plunge-frozen cyanobacterial microcolonies Panels represent en face cross-sections through a Synechococcus sp. PCC 7002 microcolony grown on dialysis tubing on top of 1% agarose A + pads. a, Close-up of cell-cell interfaces in microcolony interior shown in Fig. 2f. b, Close up of microcolony edge. Mechanical deformation of cells is more apparent in the colony interior. Asterisk denotes a cell-lysis event of a highly deformed cell. c, and d, Larger field views of representative microcolonies with distinctive difference between interior and exterior cells. Similar results were observed in two independent experiments.
Transmission electron micrographs of plunge-frozen cyanobacterial microcolonies Panels represent en face cross-sections through a Synechococcus sp. PCC 7002 microcolony grown on dialysis tubing on top of 1% agarose A + pads. a, Close-up of cell-cell interfaces in microcolony interior shown in Fig. 2f. b, Close up of microcolony edge. Mechanical deformation of cells is more apparent in the colony interior. Asterisk denotes a cell-lysis event of a highly deformed cell. c, and d, Larger field views of representative microcolonies with distinctive difference between interior and exterior cells. Similar results were observed in two independent experiments.
… 
Analysis of ∆cpc mutant a, Absorbance spectra of WT and ∆cpc strains. Consistent results were observed in three independent experiments b, Schematics of WT and ∆cpc genomic regions and location of primers to confirm segregation (not to scale). c, PCR products confirming presence of ∆cpc insert and absence of WT product. Lanes: 1, 1 kb + MW ladder (Bands representing 0.5, 0.1, 1, and 3 kilobases are marked); 2, WT (primers: cpc upstream + GmR); 3, ∆cpc (primers: cpc upstream + GmR); 4, WT (primers: cpc upstream + cpc internal); 5, ∆cpc (primers: cpc upstream + cpc internal). Consistent results were observed in two independent experiments.
Analysis of ∆cpc mutant a, Absorbance spectra of WT and ∆cpc strains. Consistent results were observed in three independent experiments b, Schematics of WT and ∆cpc genomic regions and location of primers to confirm segregation (not to scale). c, PCR products confirming presence of ∆cpc insert and absence of WT product. Lanes: 1, 1 kb + MW ladder (Bands representing 0.5, 0.1, 1, and 3 kilobases are marked); 2, WT (primers: cpc upstream + GmR); 3, ∆cpc (primers: cpc upstream + GmR); 4, WT (primers: cpc upstream + cpc internal); 5, ∆cpc (primers: cpc upstream + cpc internal). Consistent results were observed in two independent experiments.
… 
Ratio of 651 nm / 684 nm fluorescence emission from single cells during growth on 2% agarose Individual cell traces of 20 individual cells that exhibit increased fluorescence while growing on 2% agarose. Y-axis all represent values shown for top left graph. X-axis represent time elapsed from the initial frame of time-lapse imaging.
Ratio of 651 nm / 684 nm fluorescence emission from single cells during growth on 2% agarose Individual cell traces of 20 individual cells that exhibit increased fluorescence while growing on 2% agarose. Y-axis all represent values shown for top left graph. X-axis represent time elapsed from the initial frame of time-lapse imaging.
… 
Ratio of 651 nm / 684 nm emission from single cells during growth on 1% Agarose Individual cell traces of 20 individual cells from the 4-cell colony stage. Y-axis all represent values shown for top left graph. X-axis represent time elapsed from the initial frame of time-lapse imaging.
+8
Ratio of 651 nm / 684 nm emission from single cells during growth on 1% Agarose Individual cell traces of 20 individual cells from the 4-cell colony stage. Y-axis all represent values shown for top left graph. X-axis represent time elapsed from the initial frame of time-lapse imaging.
… 
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Articles
https://doi.org/10.1038/s41564-020-0684-2
1Renewable and Sustainable Energy Institute, University of Colorado, Boulder, CO, USA. 2Department of Applied Mathematics, University of Colorado,
Boulder, CO, USA. 3Biofrontiers Institute, University of Colorado, Boulder, CO, USA. 4Department of Biochemistry, University of Colorado, Boulder, CO,
USA. 5Biological Science Center, National Renewable Energy Laboratory, Golden, CO, USA. ✉e-mail: jeffrey.c.cameron@colorado.edu
Cyanobacteria are photosynthetic microorganisms that
thrive in many diverse and extreme habitats1. In response to
changes in light intensity and wavelength, temperature and
nutrient availabiliity2–6, multiple regulatory processes have evolved
to prevent the overexcitation of photosynthesis reaction centres and
the resulting production of reactive oxygen species that can damage
cellular components7–10. Cellular homeostasis is disrupted when the
available energy source (light) exceeds the cellular energy demand
(source–sink imbalance), initiating non-photochemical quenching,
alternative electron flow pathways and state transitions to balance
energy flow7,11–14. The phycobilisome—a pigment–protein complex
that funnels light energy to the photosynthetic reaction centres—
has a major role in regulating photosynthesis in cyanobacteria11,15–17.
It has remained challenging to dissect the molecular mechanisms
that regulate photosynthesis using traditional cultivation method-
ologies and ensemble-based techniques that lack the ability to track
phenotypes across individual lineages and are therefore unable to
discern subtle, albeit important, variations within a population18.
Single-cell-based technologies can overcome these limitations19–21.
However, light toxicity and increased cellular fluorescence are often
cited as major issues during live-cell imaging of cyanobacteria22.
We developed a robust imaging and computational platform
to enable quantitative analysis of cyanobacterial growth and
physiology over multiple generations under precisely controlled
environmental conditions.
While optimizing our growth and imaging system, we noticed
that mechanical interactions between cells and the growth substrate
seemed to inhibit cell growth. Mechanical forces experienced due
to cell–cell and cell–substrate interactions impact many processes
in organisms ranging from unicellular bacteria to complex multi-
cellular organisms23,24. In bacterial growth studies, frictional forces
between cells and their environment can be modified by varying
the stiffness of solid growth medium or through interactions with
the walls in microfluidics devices25,26. In heterotrophic organisms,
including Escherichia coli, an increase in frictional forces often
results in a decrease in growth rates and altered colony morpholo-
gies compared with cells grown in planktonic environments26,27.
Many cyanobacteria are motile and exhibit phototaxis in response
to certain wavelengths of light28–33 and it has been suggested that
mechanical interactions between cells can limit the growth of motile
cyanobacteria in planktonic environments34. However, much less
is known about the effect of mechanical perturbations during the
growth of non-motile cyanobacteria on solid surfaces.
We used time-lapse fluorescence microscopy, electron micros-
copy and mathematical modelling to investigate the growth and
physiology of cyanobacteria that are grown on solid substrates.
We reveal that mechanical confinement of growing cells through
cell–cell or cell–substrate interactions induces phycobilisome
detachment from the thylakoid membrane and attenuation of pho-
tosynthetic growth. Together, we show that light energy must be
converted into mechanical energy for cyanobacteria to overcome
frictional forces in their environment, in addition to being con-
verted into chemical energy for growth and cellular maintenance.
Mechanical forces therefore have a critical role in the regulation of
excessive photosynthetic light harvesting. Understanding the effects
of mechanical perturbations on cyanobacterial growth is critical for
successful long-term imaging and analysis of cyanobacterial physi-
ology at the single-cell resolution.
Results
Quantitative imaging and tracking of rapidly growing cyano-
bacteria. We utilized time-lapse fluorescence microscopy and
Mechanical regulation of photosynthesis in
cyanobacteria
Kristin A. Moore1, Sabina Altus2, Jian W. Tay 1,3, Janet B. Meehl1,3,4, Evan B. Johnson1,4,
David M. Bortz2 and Jeffrey C. Cameron 1,4,5 ✉
Photosynthetic organisms regulate their responses to many diverse stimuli in an effort to balance light harvesting with utiliz-
able light energy for carbon fixation and growth (source–sink regulation). This balance is critical to prevent the formation of
reactive oxygen species that can lead to cell death. However, investigating the molecular mechanisms that underlie the regu-
lation of photosynthesis in cyanobacteria using ensemble-based measurements remains a challenge due to population het-
erogeneity. Here, to address this problem, we used long-term quantitative time-lapse fluorescence microscopy, transmission
electron microscopy, mathematical modelling and genetic manipulation to visualize and analyse the growth and subcellular
dynamics of individual wild-type and mutant cyanobacterial cells over multiple generations. We reveal that mechanical confine-
ment of actively growing Synechococcus sp. PCC 7002 cells leads to the physical disassociation of phycobilisomes and energetic
decoupling from the photosynthetic reaction centres. We suggest that the mechanical regulation of photosynthesis is a criti-
cal failsafe that prevents cell expansion when light and nutrients are plentiful, but when space is limiting. These results imply
that cyanobacteria must convert a fraction of the available light energy into mechanical energy to overcome frictional
forces in the environment, providing insight into the regulation of photosynthesis and how microorganisms navigate their
physical environment.
NATURE MICROBIOLOGY | VOL 5 | MAY 2020 | 757–767 | www.nature.com/naturemicrobiology 757
Content courtesy of Springer Nature, terms of use apply. Rights reserved
... For example, photopatterning of topological defects in lyotropic chromonic liquid crystals via aligning elongated dye molecules on confining surfaces had to be used to guide bacteria to exhibit localized motions along only simple circular trajectories around certain types of defects 11 , similar to ones guided by concentric director patterns in lyotropic liquid crystals of DNA 10 . On the other hand, one of the most common lifeforms on Earth, cyanobacteria use light as an energy source derived through photosynthetic activity, which once transformed our Earth's atmosphere while generating oxygen and converting carbon dioxide into biomass [34][35][36][37][38][39][40][41][42][43][44] . They also might be the first bacteria to be discovered and directly observed in a microscope 44 , with the very first historical microbiology reports mentioning the light-powered activity of filaments consisting of "green globules joined together" and moving "in an orderly manner" 38,41,44 . ...
... They also might be the first bacteria to be discovered and directly observed in a microscope 44 , with the very first historical microbiology reports mentioning the light-powered activity of filaments consisting of "green globules joined together" and moving "in an orderly manner" 38,41,44 . Such light-powered active matter systems may offer unprecedented control of the out-of-equilibrium behavior, potentially even in relation to mats, blooms and production of oxygen or toxins [34][35][36][37][38][39][40] . Surprisingly, active nematic behavior of cyanobacterial filaments remained quantitatively unexplored, with the great potential of controlling it by light and gradients of its intensity never utilized. ...
... Furthermore, we explore interactions of the locally induced active nematic's orientational order and bacterial motility with edges of illuminated sample areas and with immobile foreign inclusions, showing emergence of boojum defects. Our findings may allow for designing highly controlled experiments to test active matter theories and may provide insights for commanding the out-of-equilibrium collective behavior of cyanobacterial active matter 60 , with potential utility including control of bacterial mats and blooms, as well as the ensuing oxygen generation and inhibition of toxin production [34][35][36][37][38][39][40] . ...
Photosynthetically-powered phototactic active nematic liquid crystal fluids and gels
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One of the most ancient forms of life dating to ~3.5 billion years ago, cyanobacteria are highly abundant organisms that convert light into energy and motion, often within conjoined filaments and larger colonies that attract a great deal of interest but their active nematic behavior remained unexplored. Here we demonstrate how light causes a spontaneous self-assembly of two- and three-dimensional active nematic states of cyanobacterial filaments, with a plethora of topological defects. We quantify light-controlled evolutions of orientational and velocity order parameters during the transition between disordered and orientationally ordered states of photosynthetic active matter, as well as the subsequent active nematic’s fluid-gel transformation. Patterned illumination and foreign inclusions with different shapes interact with cyanobacterial active nematics in nontrivial ways while inducing interfacial boundary conditions and fractional boojum defects. Our phototactic model system promises opportunities to systematically explore fundamental properties and technological utility of the liquid crystalline active matter.
View
... When coupled to PSII, phycobilisomes act as an energy funnel, directing light energy absorbed by the rods to the central core of the phycobilisome and the PSII reaction center (Zheng 2021). Reduced absorption cross section of PSII resulting from antenna truncation leads to light limitation and reduced growth compared to the WT under typical growth conditions (Liberton et al. 2013;Kirst et al. 2014;Moore et al. 2020), making it difficult to directly compare the physiology and light response of these strains in bulk culture. Recently, adaptive laboratory evolution studies under highlight conditions selected for strains with reduced levels of antenna (Dann 2021). ...
... The two strains were grown overnight in separate liquid cultures, then mixed and spotted onto an agarose pad (0.5% w/v A + media) (Extended Data Fig. 1 in Supplementary material). The Δcpc strain was previously shown to be mechanically sensitive to agarose concentrations > 0.5% (Moore et al. 2020). The pad was placed into a glass-bottomed imaging dish (µ-Dish, Ibidi), which was then inserted into a temperature-controlled chamber on a mechanized fluorescence microscope (Nikon TiE) and allowed to incubate for 30 min to acclimatize the cells to the new environment. ...
... The pad was placed into a glass-bottomed imaging dish (µ-Dish, Ibidi), which was then inserted into a temperature-controlled chamber on a mechanized fluorescence microscope (Nikon TiE) and allowed to incubate for 30 min to acclimatize the cells to the new environment. During this incubation period, the cells were illuminated with a red LED (610-650 nm) at an intensity of ~ 157 µmol photons m −2 s −1 (Lida light engine, Lumencore), which was previously determined to be optimal for microscopic growth of PCC 7002 (Moore et al. 2020;Hill et al. 2020). Following this initial incubation period, the cells were imaged for 10 h. ...
Asymmetric survival in single-cell lineages of cyanobacteria in response to photodamage
Article
Full-text available
  • Dec 2022
  • PHOTOSYNTH RES
Oxygenic photosynthesis is driven by the coupled action of the light-dependent pigment–protein complexes, photosystem I and II, located within the internal thylakoid membrane system. However, photosystem II is known to be prone to photooxidative damage. Thus, photosynthetic organisms have evolved a repair cycle to continuously replace the damaged proteins in photosystem II. However, it has remained difficult to deconvolute the damage and repair processes using traditional ensemble approaches. Here, we demonstrate an automated approach using time-lapse fluorescence microscopy and computational image analysis to study the dynamics and effects of photodamage in single cells at subcellular resolution in cyanobacteria. By growing cells in a two-dimensional layer, we avoid shading effects, thereby generating uniform and reproducible growth conditions. Using this platform, we analyzed the growth and physiology of multiple strains simultaneously under defined photoinhibitory conditions stimulated by UV-A light. Our results reveal an asymmetric cellular response to photodamage between sibling cells and the generation of an elusive subcellular structure, here named a ‘photoendosome,’ derived from the thylakoid which could indicate the presence of a previously unknown photoprotective mechanism. We anticipate these results to be a starting point for further studies to better understand photodamage and repair at the single-cell level.
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... Photosynthesis, as a crucial physiological process on Earth, serves as the fundamental basis for the sustenance of the biosphere. In recent years, research on photosynthesis has advanced significantly, leading to notable breakthroughs in the analysis of photosynthetic structure [1] and the elucidation of the genetic mechanisms underlying photosynthesis [2][3][4][5]. With the advancement of chlorophyll fluorescence technology, the investigation of photosynthesis has witnessed a new breakthrough through the analysis of photosynthetic phenotypes, including chlorophyll fluorescence parameters [6,7]. ...
... Additionally, it was found that the samples with genotype GA exhibited a higher degree of environmental disturbance. Based on the analysis of the genetic effect of the hub SNP 4289989 (Fig. 7E), the effect curve exhibited an initial increase within the range of low light intensity (2)(3) and subsequently decreased with the changing gradient light intensity. Moreover, the trend and variation range of the independent genetic effect curves were essentially similar to those of the overall curves. ...
Computational dissection of genetic variation modulating the response of multiple photosynthetic phenotypes to the light environment
Article
Full-text available
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  • BMC GENOMICS
Background The expression of biological traits is modulated by genetics as well as the environment, and the level of influence exerted by the latter may vary across characteristics. Photosynthetic traits in plants are complex quantitative traits that are regulated by both endogenous genetic factors and external environmental factors such as light intensity and CO2 concentration. The specific processes impacted occur dynamically and continuously as the growth of plants changes. Although studies have been conducted to explore the genetic regulatory mechanisms of individual photosynthetic traits or to evaluate the effects of certain environmental variables on photosynthetic traits, the systematic impact of environmental variables on the dynamic process of integrated plant growth and development has not been fully elucidated. Results In this paper, we proposed a research framework to investigate the genetic mechanism of high-dimensional complex photosynthetic traits in response to the light environment at the genome level. We established a set of high-dimensional equations incorporating environmental regulators to integrate functional mapping and dynamic screening of gene‒environment complex systems to elucidate the process and pattern of intrinsic genetic regulatory mechanisms of three types of photosynthetic phenotypes of Populus simonii that varied with light intensity. Furthermore, a network structure was established to elucidate the crosstalk among significant QTLs that regulate photosynthetic phenotypic systems. Additionally, the detection of key QTLs governing the response of multiple phenotypes to the light environment, coupled with the intrinsic differences in genotype expression, provides valuable insights into the regulatory mechanisms that drive the transition of photosynthetic activity and photoprotection in the face of varying light intensity gradients. Conclusions This paper offers a comprehensive approach to unraveling the genetic architecture of multidimensional variations in photosynthetic phenotypes, considering the combined impact of integrated environmental factors from multiple perspectives.
View
... Deletion of slr1916, likely codes for esterase, increased PSI content under HL conditions whereas the mutation in hik26, encoding the two-component sensor histidine kinase, was suggested to affect the regulation of the expression levels of HL-responsive genes. 14 Until now, more than 100 proteins involved in gene transcription, metabolism, and photosynthesis have been reported to be associated with HL tolerance in microalgae, 15 suggesting that mutations in some genes may alter their response to HL stress. ...
... 10 The cyanobacterial PSI structure is rich in zeaxanthin, ⊎-carotene, and echinenone. 15 Multiple studies have described the exact locations and structural importance of carotenoids in PSI and PSII. 34 The expression levels of ipi, crtO, crtR, and important PSI structural genes were significantly affected by the deletion of slr0681. ...
The Na/Ca antiporter slr0681 affects carotenoid production in Synechocystis sp. PCC 6803 under high‐light stress
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BACKGROUND Carotenoids play key roles in photosynthesis and are widely used in foods as natural pigments, antioxidants, and health‐promoting compounds. Enhancing carotenoid production in microalgae via biotechnology has become an important area of research. RESULTS We knocked out the Na⁺/Ca²⁺ antiporter gene slr0681 in Synechocystis sp. PCC 6803 via homologous recombination and evaluated the effects on carotenoid production under normal (NL) and high‐light (HL) conditions. On day 7 of NL treatment in calcium ion (Ca²⁺)‐free medium, the cell density of Δslr0681 decreased by 29% compared to the wild type (WT). After 8 days of HL treatment, the total carotenoid contents decreased by 35% in Δslr0681, and the contents of individual carotenoids were altered: myxoxanthophyll, echinenone, and β‐carotene contents increased by 10%, 50%, and 40%, respectively, while zeaxanthin contents decreased by ~40% in Δslr0681 versus the WT. The expression patterns of carotenoid metabolic pathway genes also differed: ipi expression increased by 1.2‐ to 8.5‐fold, whereas crtO and crtR expression decreased by ~90% and 60%, respectively, in ∆slr0681 versus the WT. In addition, in ∆slr0681, the expression level of psaB (encoding a photosystem I structural protein) doubled, whereas the expression levels of the photosystem II genes psbA2 and psbD decreased by ~53% and 84%, respectively, compared to the WT. CONCLUSION These findings suggest that slr0681 plays important roles in regulating carotenoid biosynthesis and structuring of the photosystems in Synechocystis sp. This study provides a theoretical basis for the genetic engineering of microalgae photosystems to increase their economic benefits and lays the foundation for developing microalgae germplasm resources with high carotenoid contents. © 2023 Society of Chemical Industry.
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... We initially constructed a CO 2 sequestration module that converted CO 2 into an intermediate carbohydratesucrose. [9] Sucrose permease CscB is a sucrose/H + symporter that facilitates sucrose transport along the proton gradient. [10] We evaluated the effect of introducing sucrose permease encoding gene cscB into different neutral sites in Synechococcus elongatus (photosynthetic organism) to test the capacity of sucrose secretion ( Figure S1). ...
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Computational dissection of genetic variation modulating the response of multiple photosynthetic phenotypes to the light environment
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View
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Full-text available
  • Mar 2018
Cyanobacteria are photosynthetic microorganisms whose metabolism can be modified through genetic engineering for production of a wide variety of molecules directly from CO2, light, and nutrients. Diverse molecules have been produced in small quantities by engineered cyanobacteria to demonstrate the feasibility of photosynthetic biorefineries. Consequently, there is interest in engineering these microorganisms to increase titer and productivity to meet industrial metrics. Unfortunately, differing experimental conditions and cultivation techniques confound comparisons of strains and metabolic engineering strategies. In this work, we discuss the factors governing photoautotrophic growth and demonstrate nutritionally replete conditions in which a model cyanobacterium can be grown to stationary phase with light as the sole limiting substrate. We introduce a mathematical framework for understanding the dynamics of growth and product secretion in light-limited cyanobacterial cultures. Using this framework, we demonstrate how cyanobacterial growth in differing experimental systems can be easily scaled by the volumetric photon delivery rate using the model organisms Synechococcus sp. strain PCC7002 and Synechococcus elongatus strain UTEX2973. We use this framework to predict scaled up growth and product secretion in 1L photobioreactors of two strains of Synechococcus PCC7002 engineered for production of L-lactate or L-lysine. The analytical framework developed in this work serves as a guide for future metabolic engineering studies of cyanobacteria to allow better comparison of experiments performed in different experimental systems and to further investigate the dynamics of growth and product secretion.
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Ecogenomics and Taxonomy of Cyanobacteria Phylum
Article
Full-text available
  • Nov 2017
Cyanobacteria are major contributors to global biogeochemical cycles. The genetic diversity among Cyanobacteria enables them to thrive across many habitats, although only a few studies have analyzed the association of phylogenomic clades to specific environmental niches. In this study, we adopted an ecogenomics strategy with the aim to delineate ecological niche preferences of Cyanobacteria and integrate them to the genomic taxonomy of these bacteria. First, an appropriate phylogenomic framework was established using a set of genomic taxonomy signatures (including a tree based on conserved gene sequences, genome-to-genome distance, and average amino acid identity) to analyse ninety-nine publicly available cyanobacterial genomes. Next, the relative abundances of these genomes were determined throughout diverse global marine and freshwater ecosystems, using metagenomic data sets. The whole-genome-based taxonomy of the ninety-nine genomes allowed us to identify 57 (of which 28 are new genera) and 87 (of which 32 are new species) different cyanobacterial genera and species, respectively. The ecogenomic analysis allowed the distinction of three major ecological groups of Cyanobacteria (named as i. Low Temperature; ii. Low Temperature Copiotroph; and iii. High Temperature Oligotroph) that were coherently linked to the genomic taxonomy. This work establishes a new taxonomic framework for Cyanobacteria in the light of genomic taxonomy and ecogenomic approaches.
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Light-controlled motility in prokaryotes and the problem of directional light perception
Article
Full-text available
  • Oct 2017
  • FEMS MICROBIOL REV
The natural light environment is important to many prokaryotes. Most obviously, phototrophic prokaryotes need to acclimate their photosynthetic apparatus to the prevailing light conditions, and such acclimation is frequently complemented by motility to enable cells to relocate in search of more favorable illumination conditions. Non-phototrophic prokaryotes may also seek to avoid light at damaging intensities and wavelengths, and many prokaryotes with diverse lifestyles could potentially exploit light signals as a rich source of information about their surroundings and a cue for acclimation and behavior. Here we discuss our current understanding of the ways in which bacteria can perceive the intensity, wavelength and direction of illumination, and the signal transduction networks that link light perception to the control of motile behavior. We discuss the problems of light perception at the prokaryotic scale, and the challenge of directional light perception in small bacterial cells. We explain the peculiarities and the common features of light-controlled motility systems in prokaryotes as diverse as cyanobacteria, purple photosynthetic bacteria, chemoheterotrophic bacteria and haloarchaea.
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Phototaxis in a wild isolate of the cyanobacterium Synechococcus elongatus
Article
  • Dec 2018
Many cyanobacteria, which use light as an energy source via photosynthesis, have evolved the ability to guide their movement toward or away from a light source. This process, termed “phototaxis,” enables organisms to localize in optimal light environments for improved growth and fitness. Mechanisms of phototaxis have been studied in the coccoid cyanobacterium Synechocystis sp. strain PCC 6803, but the rod-shaped Synechococcus elongatus PCC 7942, studied for circadian rhythms and metabolic engineering, has no phototactic motility. In this study we report a recent environmental isolate of S. elongatus , the strain UTEX 3055, whose genome is 98.5% identical to that of PCC 7942 but which is motile and phototactic. A six-gene operon encoding chemotaxis-like proteins was confirmed to be involved in phototaxis. Environmental light signals are perceived by a cyanobacteriochrome, PixJ Se (Synpcc7942_0858), which carries five GAF domains that are responsive to blue/green light and resemble those of PixJ from Synechocystis . Plate-based phototaxis assays indicate that UTEX 3055 uses PixJ Se to sense blue and green light. Mutation of conserved functional cysteine residues in different GAF domains indicates that PixJ Se controls both positive and negative phototaxis, in contrast to the multiple proteins that are employed for implementing bidirectional phototaxis in Synechocystis .
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Selective Permeability of Carboxysome Shell Pores to Anionic Molecules
Article
  • Sep 2018
Carboxysomes are closed polyhedral cellular microcompartments that increase the efficiency of carbon fixation in autotrophic bacteria. Carboxysome shells consist of small proteins that form hexameric units with semi-permeable central pores containing binding sites for anions. This feature is thought to selectively allow access to RuBisCO enzymes inside the carboxysome by HCO3⁻ (the dominant form of CO2 in the aqueous solution at pH 7.4) but not O2, which leads to a non-productive reaction. To test this hypothesis, here we use molecular dynamics simulations to characterize the energetics and permeability of CO2, O2, and HCO3⁻ through the central pores of two different shell proteins, namely, CsoS1A of α-carboxysome and CcmK4 of β-carboxysome shells. We find that the central pores are in fact selectively permeable to anions such as HCO3⁻, as predicted by the model.
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Voltage-gated calcium flux mediates Escherichia coli mechanosensation
Article
  • Aug 2017
Significance Bacteria cope with changing external environments and must therefore sense and respond to their local conditions. In addition to sensing numerous chemical cues, in this paper we show that Escherichia coli can sense the local mechanical environment through voltage-induced calcium flux. This mechanism is similar to sensory neurons in vertebrates, suggesting an ancient process of voltage-regulated mechanotransduction. Mechanical contact drives pathogenicity in several species of bacteria and we now propose a potential mechanism for this sensation.
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