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Pentoses Used in Cultures of Synechococcus nidulans and Spirulina paracas: Evaluation of Effects in Growth and in Content of Proteins and Carbohydrates

Abstract

Abstract

The biological assimilation of the sugars present in lignocellulosic residues has gained prominence since these residues are the most abundant and economic residues in nature. Thus, the objective of this work was to determine whether the use of D-xylose and L-arabinose as sources of carbon in Synechococcus nidulans and Spirulina paracas cultures affects the growth and production of proteins and carbohydrates. Kinetic growth parameters, pentose consumption, protein content and carbohydrates were evaluated. Synechococcus nidulans and Spirulina paracas consumed all concentrations of pentose used. The highest cellular concentration (1.37 g.L-1) and the highest protein productivity (54 mg.L-1.d-1) were obtained for Spirulina paracas, which was submitted to the addition of 38.33 mg.L-1 D-xylose and 1.79 mg.L-1 L-arabinose. The use of pentose promoted the accumulation of proteins for the studied microalgae. This is one of the first works to report protein bioaccumulation as a result of pentose addition.

Keywords:
arabinose; proteins; Spirulina; Synechococcus; xylose


INTRODUCTION

New strategies to reformulate specific culture growth conditions are of great interest to raise the productivity of different species of microalgae. In the search for alternative carbon sources for microalgae culture, pentoses are interesting [11 Freitas BCB, Esquível MG, Matos RG, et al. Nitrogen balancing and xylose addition enhances growth capacity and protein content in Chlorella minutissima cultures. Bioresour Technol. 2016;218:129–33.] since the most abundant global renewal biomass source is lignocellulosic material, which contains significant amounts of pentose [22 Sindhu R, Binod P, Pandey A. Biological pretreatment of lignocellulosic biomass – an overview. Bioresour Technol. 2016;199:76–82.].

With a higher interest in the conversion of vegetal biomass to bioproducts, studies on pentose catabolism, which includes the catabolism of L-arabinose and D-xylose, have drawn attention, and only for the last few years, wild species that are capable of using pentose have been isolated and studied [33 Seiboth B, Metz B. Fungal arabinan and L-arabinose metabolism. Appl Microbiol Biotechnol. 2011;89:1665–73.]. The utilization of pentose by microalgae is an in-development technology due to scarce studies related to the metabolic routes involved in the process of assimilation. Zheng et al [44 Zheng Y, Yu X, Li T, et al. Induction of D-xylose uptake and expression of NAD(P)H-linked xylose reductase and NADP + -linked xylitol dehydrogenase in the oleaginous microalga Chlorella sorokiniana. Biotechnol Biofuels. 2014;7:125.] showed that the assimilation of xylose increases gradually with the activation of intermembrane transporters.

Recently associated with the use of pentose, studies with modification of the cultures’ physical conditions, such as light intensity, have been developed [55 Freitas BCB, Cassuriaga APA, Morais MG, et al. Pentoses and light intensity increase the growth and carbohydrate production and alter the protein profile of Chlorella minutissima. Bioresour Technol. 2017;238:248–53.], as well as the use of a combination with other carbon sources, such as carbon dioxide (CO2) in Chlorella minutissima [66 Freitas BCB, Morais MG, Costa JAV. Chlorella minutissima cultivation with CO2 and pentoses: Effects on kinetic and nutritional parameters. Bioresour Technol. 2017;244:338–44.]. For microalgae of the Chlorella genus, studies involving modifications in the protein profile resulting from the addition of pentose have also gained visibility [55 Freitas BCB, Cassuriaga APA, Morais MG, et al. Pentoses and light intensity increase the growth and carbohydrate production and alter the protein profile of Chlorella minutissima. Bioresour Technol. 2017;238:248–53., 66 Freitas BCB, Morais MG, Costa JAV. Chlorella minutissima cultivation with CO2 and pentoses: Effects on kinetic and nutritional parameters. Bioresour Technol. 2017;244:338–44.]. The use of pentose has also been reported as responsible for lipid bioaccumulation by microalgae [77 Leite GB, Paranjape K, Hallenbeck PC. Breakfast of champions : Fast lipid accumulation by cultures of Chlorella and Scenedesmus induced by xylose. Algal Res. 2016;16:338–48., 88 Leite GB, Paranjape K, Abdelaziz AEM, et al. Utilization of biodiesel-derived glycerol or xylose for increased growth and lipid production by indigenous microalgae. Bioresour Technol. 2015;184:123–30.].

Therefore, the use of pentose, which is considered a low-value sub product, for the production of compounds with high added value in microalgae collaborates the development of sustainable production systems. The number of studies about the use of pentose in microalgae is still low, and they have been focused on species from the Chlorophyta division (especially microalgae from the Chlorella genus)[55 Freitas BCB, Cassuriaga APA, Morais MG, et al. Pentoses and light intensity increase the growth and carbohydrate production and alter the protein profile of Chlorella minutissima. Bioresour Technol. 2017;238:248–53., 66 Freitas BCB, Morais MG, Costa JAV. Chlorella minutissima cultivation with CO2 and pentoses: Effects on kinetic and nutritional parameters. Bioresour Technol. 2017;244:338–44., 88 Leite GB, Paranjape K, Abdelaziz AEM, et al. Utilization of biodiesel-derived glycerol or xylose for increased growth and lipid production by indigenous microalgae. Bioresour Technol. 2015;184:123–30., 99 Freitas BCB, Brächer EH, de Morais EG, et al. Cultivation of different microalgae with pentose as carbon source and the effects on the carbohydrate content. Environ Technol. 2017;3330:1–9.].

Thereby, it is necessary to assess the pentose usage capacity of other species with different cellular structures. Thus, the objective of this work was to assess whether the use of D-Xylose or L-Arabinose as a carbon source in Synechococcus nidulans and Spirulina paracas cultures affects the growth and production of proteins and carbohydrates.

MATERIAL AND METHODS

Microalgae and culture conditions

To perform the assays, Synechococcus nidulans and Spirulina paracas from the Collection of the Laboratory of Biochemical Engineering of the Federal University of Rio Grande (FURG), Rio Grande do Sul, Brazil, were used.

Zarrouk medium [1010 Zarrouk C. Contribution à l’étude d’une cyanophycée. Influence de divers facteurs physiques et chimiques sur la croissance et photosynthèse de Spirulina maxima Geitler. University of Paris; 1966.] with no carbon source (NaHCO3), pH=9,5 (correction with solutions of NaOH) and reduced nitrogen concentration (0.125 g.L-1 NaNO3) was used for the cultures with pentose additions. For the control culture, Zarrouk medium [1010 Zarrouk C. Contribution à l’étude d’une cyanophycée. Influence de divers facteurs physiques et chimiques sur la croissance et photosynthèse de Spirulina maxima Geitler. University of Paris; 1966.] without alterations was used.

To evaluate the microalgae growth, cultivations were conducted in Erlenmeyer-type photobioreactors with a total volume of 2 L and a working volume of 1.8 L and performed in duplicate, with a triplicate of the analysis. The temperature was 30° C, the photoperiod was 12 h light/12 h dark, and an illuminance of 33.75 μmol.m-2.s-1 was provided by fluorescent lamps (40 W). The cultures were maintained until the stationary phase of growth.

The addition of D-xylose and L-arabinose (Vetec Quimica, Sigma, Aldrich Corporation) was performed using a synthetic broth, which had concentrations of pentoses that were equivalent to their concentrations in the hydrolyzate broth of pretreated sugarcane bagasse (Table 1), as previously proposal by Freitas et al [99 Freitas BCB, Brächer EH, de Morais EG, et al. Cultivation of different microalgae with pentose as carbon source and the effects on the carbohydrate content. Environ Technol. 2017;3330:1–9.].

Table 1
Concentrations of D-xylose and L-arabinose in Zarrouk medium.

Growth parameters

Cell concentration was determined by spectrophotometry using a previously established standard curve for Synechococcus nidulans and Spirulina paracas. These curves were obtained at 670 nm using a spectrophotometer (QUIMIS Q798DRM, Diadema, SP, Brazil) and correlated the relative optical density and dry biomass weight, as previously proposed by Costa et al [1111 Costa JAV, Colla LM, Filho PD. Modelling of Spirulina platensis growth in fresh water using response surface methodology. World J Microbiol Biotechnol. 2002;1:603–7.].

The biomass productivity (Pmax, g.L-1.d-1) was obtained from the equation Pmax = (Xt - X0)/(t - t0), where Xt is the biomass concentration (g.L-1) at time t (d), and X0 is the biomass concentration (g.L-1) at time t0 (d). The maximum specific growth rate (μmax, d-1) was determined using an exponential regression applied to the logarithmic growth phase.

Determination the consumption of pentoses

Pentose consumption was determined using the methodology proposed by Somogyi [1212 Somogyi M. Notes on Sugar Determination. J Biol Chem. 1952;195:19–23.] and was applied to the supernatant obtained by centrifugation of the cultures at 27,000×g for 10 min.

Harvesting biomass

The biomass was separated from the culture medium and the washing water by centrifugation at 15,000×g and 15 °C for 20 min. Then, the precipitate was dried for 24 h at 50 °C.

Carbohydrate and protein content

The total carbohydrate concentration in biomass (%w.w-1) was determined using the method 3.5 -DNS [1313 Miller GL. Use of dinitrosalicylic acid for determination of reducing sufar. Anal Chem. 1959;E-31:420–8.].

The proteins were quantified by the micro-Kjeldahl method according to the methodology described by AOAC [1414 AOAC. Official Methods of Analysis of the Association of Official Analytical Chemists. 17th ed. Maryland; 2000.].

The carbohydrate (PCHO, mg.L-1.d-1) and protein (PPROT, mg.L-1.d-1) productivities were calculated based on the dried biomass, as described in Equations 1 and 2, respectively, where Xf is the final biomass concentration of a culture (g.L-1), CHO is the carbohydrate content (%), PROT is the protein content (%), and ∆t is the cultivation time (d).

P CHO (g .L -1 .d -1 )= CHO . X f 100 . Δ t (1)
P PROT (g .L -1 .d -1 )= PROT . X f 100 . Δ t (2)

The results of the characterization of the biomass obtained from cultures with pentoses (CC5) relative to that obtained from control cultures (CC) were compared according to the relationship R=((CC5-CC)/(CC)).100, where R (RC or RP) corresponds to the percentage difference in the results obtained with pentoses relative to the results obtained in the control cultures.

Statistical analyses

An analysis of variance and Tukey's test were performed, with a confidence level of 95% (p>0.05), to determine the differences between the means in each assay.

RESULTS AND DISCUSSION

Higher concentrations of D-xylose and L-arabinose provided to the cultures of Synechococcus nidulans as a carbon source delayed a possible stationary phase due to the use of the traditional carbon source in Zarrouk medium (NaHCO3) (Figure 1a), while for Spirulina paracas, lower concentrations of pentose (1, 5 and 10%) were capable of promoting growth for longer periods of time (Figure 1b). This behavior can be related to the maintenance of the enzymes that either delay or modify the arrival into the stationary growth phase, which occur with the use of different carbon sources at adequate conditions and concentrations [1515 Ores J da C, Amarante MCA de, Kalil SJ. Co-production of carbonic anhydrase and phycobiliproteins by Spirulina sp. and Synechococcus nidulans. Bioresour Technol. 2016;219:219–27.].

Figure 1
Growth of Synechococcus nidulans and Spirulina paracas under different culture conditions.

For the assimilation of pentose, specific metabolic routes that aid in the pentose intermembrane transport, such as D-xylose [44 Zheng Y, Yu X, Li T, et al. Induction of D-xylose uptake and expression of NAD(P)H-linked xylose reductase and NADP + -linked xylitol dehydrogenase in the oleaginous microalga Chlorella sorokiniana. Biotechnol Biofuels. 2014;7:125.], have been reported. Other forms of pentose absorption by microalgae can also happen through the activation of sugar transporters [1616 Yang S, Liu G, Meng Y, et al. Utilization of xylose as a carbon source for mixotrophic growth of Scenedesmus obliquus. Bioresour Technol. 2014;172:180–5.]. For S. paracas and S. nidulans, at every pentose concentration, a quick consumption of those sugars was verified. The total consumption of the lowest concentrations (1 and 5% C5) occurred at the first day of culture. At the end of the fourth day, the highest concentrations had already been consumed by the strains of cyanobacteria. The fast consumption of these nutrient sources is related to the low pentose concentrations used in replacement of sodium bicarbonate from the Zarrouk medium. Leite et al [77 Leite GB, Paranjape K, Hallenbeck PC. Breakfast of champions : Fast lipid accumulation by cultures of Chlorella and Scenedesmus induced by xylose. Algal Res. 2016;16:338–48.] also report a quick adaptation and pentose consumption by microalgae from the Scenedesmaceae and Chlorophyceae families. Freitas et al [55 Freitas BCB, Cassuriaga APA, Morais MG, et al. Pentoses and light intensity increase the growth and carbohydrate production and alter the protein profile of Chlorella minutissima. Bioresour Technol. 2017;238:248–53., 66 Freitas BCB, Morais MG, Costa JAV. Chlorella minutissima cultivation with CO2 and pentoses: Effects on kinetic and nutritional parameters. Bioresour Technol. 2017;244:338–44.] report the consumption of 20 mg.L-1 pentose for a maximum of 3 days for Chlorella minutissima.

S. paracas showed a higher cellular concentration (1.37 g.L-1) for the assays with the addition of 20% of pentose and reduction of 50% in the nitrogenous component, even in the face of controlling conditions. That higher biomass production is a result of the pentose positive contribution in the C/N relation, which was already demonstrated by Freitas et al[11 Freitas BCB, Esquível MG, Matos RG, et al. Nitrogen balancing and xylose addition enhances growth capacity and protein content in Chlorella minutissima cultures. Bioresour Technol. 2016;218:129–33.] and Freitas et al [55 Freitas BCB, Cassuriaga APA, Morais MG, et al. Pentoses and light intensity increase the growth and carbohydrate production and alter the protein profile of Chlorella minutissima. Bioresour Technol. 2017;238:248–53.] when the nitrogen source is reduced.

The highest productivities and specific growth rates for S. paracas were 0.13 g.L-1.d-1 and 0.24 d-1, respectively, and both in cultures with 10% C5 (Table 2). For S. nidulans, control cultures resulted in better productivity responses and growth rates (Table 2).

Table 2
Results for the maximum cell concentration (Xmax, g.L-1), maximum productivity (Pmax, g.L-1.d-1), maximum specific growth rate (μmax, d-1), carbohydrate (%w.w-1) and protein (%w.w-1) contents, productivity of protein (PPROT) and carbohydrates (PCHO) (mg.L-1.d-1) (mean±standard deviation) and difference in carbohydrate (RC-%) and protein (RP-%) contents generated by the addition of pentoses under different Synechococcus nidulans and Spirulina paracas culture conditions compared to the control assays.

The addition of 30% C5 resulted in a larger decline in biomass productivity for S. nidulans (Table 2). Many studies showed that a difference in the productivity between similar species occurs when cultures are started at different concentrations [1717 Chow TJ, Su HY, Tsai TY, et al. Using recombinant cyanobacterium (Synechococcus elongatus) with increased carbohydrate productivity as feedstock for bioethanol production via separate hydrolysis and fermentation process. Bioresour Technol. 2015;184:33–41., 1818 Lanlan Z, Lin C, Junfeng W, et al. Attached cultivation for improving the biomass productivity of Spirulina platensis. Bioresour Technol. 2015;181:136–42.]. Since all experiments started with a cellular concentration of 0.2 g.L-1 in this study, the addition of pentose can be considered the limiting factor for the difference between the obtained results for the studied strains.

The addition of pentose created a proper environment for the synthesis of proteins, which is observed with the positive (Rp) effect from the use of pentose for S. nidulans and S. paracas shown in Table 2. The highest content of determined protein was 62.9% for S. nidulans that was grown with the addition of 10% C5, and this protein content was the result of a raise of 46.3% (RP) in comparison to the control assay (Table 2). The use of 20% pentose induced the accumulation of 52.9% of proteins by S. paracas (Table 2). Since macromolecule productivity is related to the biomass production, the higher protein productivity determined for S. paracas (54 mg.L-1.d-1) followed the higher cellular growth (1.37 g.L-1) found for 20% C5 (Table 2).

The effects of xylose in the growth of three wild strains of Chlorella vulgaris were reported by Leite et al [77 Leite GB, Paranjape K, Hallenbeck PC. Breakfast of champions : Fast lipid accumulation by cultures of Chlorella and Scenedesmus induced by xylose. Algal Res. 2016;16:338–48.]. For these authors [77 Leite GB, Paranjape K, Hallenbeck PC. Breakfast of champions : Fast lipid accumulation by cultures of Chlorella and Scenedesmus induced by xylose. Algal Res. 2016;16:338–48.], the addition of xylose presented similar results for those three Chlorella strains, inducing a rapid accumulation of lipids under mixotrophic conditions, suggesting that relatively low quantities of xylose can act as an intensifier of lipid production. The accumulation of carbohydrates and the concentration reduction of proteins in Chlorella minutissima cells caused by the addition of pentose were reported by Freitas et al [55 Freitas BCB, Cassuriaga APA, Morais MG, et al. Pentoses and light intensity increase the growth and carbohydrate production and alter the protein profile of Chlorella minutissima. Bioresour Technol. 2017;238:248–53.]. In this study [55 Freitas BCB, Cassuriaga APA, Morais MG, et al. Pentoses and light intensity increase the growth and carbohydrate production and alter the protein profile of Chlorella minutissima. Bioresour Technol. 2017;238:248–53.], the use of 20 mg.L-1 arabinose raised the carbohydrate content to 53%, whereas the use of xylose and arabinose combined resulted in a loss of 38% in the protein content of C. minutissima.

Unlike what has been reported for Chlorella cells by Leite et al [77 Leite GB, Paranjape K, Hallenbeck PC. Breakfast of champions : Fast lipid accumulation by cultures of Chlorella and Scenedesmus induced by xylose. Algal Res. 2016;16:338–48.] and Freitas et al [55 Freitas BCB, Cassuriaga APA, Morais MG, et al. Pentoses and light intensity increase the growth and carbohydrate production and alter the protein profile of Chlorella minutissima. Bioresour Technol. 2017;238:248–53.], for S. nidulans and S. paracas, the pentoses acted as inducers in the biomass conversion for protein production. This biomolecule production difference can be related to cellular organization and the differences in the complexity of molecular mechanisms utilized by different groups since cyanobacteria (Synechococcus and Spirulina) are prokaryotes, whereas microalgae from the Chlorella genus are eukaryotes. Since differences in photosynthetic metabolism can directly affect nutrient assimilation and biomolecule production, one of the factors that can explain the difference in the response to the pentose addition is that cyanobacteria contain two photosynthetic systems that operate in sequence and are able to perform oxygenic photosynthesis. Other groups contain only one type of reaction center, I or II, depending on the taxon [1919 Nowicka B, Kruk J. Powered by light: Phototrophy and photosynthesis in prokaryotes and its evolution. Microbiol Res. 2016;186–187:99–118., 2020 Zeng Y, Feng F, Medova H, et al. Functional type 2 photosynthetic reaction centers found in the rare bacterial phylum Gemmatimonadetes. Proc Natl Acad Sci. 2014;111:7795–800.].

The carbohydrate content of S. nidulans and S. paracas was reduced at all of the studied pentose concentrations. This effect is suggested through the negative values obtained for the effect of the pentose (RC - Table 2). Another factor that demonstrates that pentose has a negative effect on carbohydrate production in cyanobacteria is that the highest carbohydrate productivities were obtained for the control culture conditions (without substituting NaHCO3 for pentose) for both microalgae (Table 2). The most evident reduction in the content of carbohydrates (-132,9%) was verified for S. paracas under the addition of 5% pentose (Table 2).

Both cyanobacteria strains studied showed a capacity for modifying the cells’ biochemical composition and increasing their growth rates through the variation in culture conditions resulting from the use of D-xylose and L-arabinose. Those results indicate that the addition of these sugars can positively collaborate with the photosynthetic rates, converging on protein accumulation alongside the growth of the studied strains.

CONCLUSION

The cellular growth and the protein productivity of Spirulina paracas were positively influenced by the addition of 20% pentose, reaching 1.37 g.L-1 biomass and 54 mg.L-1.d-1 proteins. For Synechococcus nidulans, the highest stimulus in biomolecule production resulted from the addition of 10% pentose, which led to a protein content of 62.9%. The usage of pentose in place of traditionally employed carbon sources in cyanobacteria cultures can be considered a viable strategy for the growth and the production of bioproducts as proteins for Synechococcus nidulans and Spirulina paracas.

Acknowledgments:

The authors would like to thank the Coordination for the Improvement of Higher Education Personnel (CAPES), the National Council for Scientific and Technological Development (CNPq), and the Ministry of Science, Technology, Innovations and Communication (MCTIC) for the financial support provided and the Program to Support Production of Publication Academic/PROPESP/ FURG/2018.

HIGHLIGHTS

  • • Pentose promotes Synechococcus and Spirulina growth.
  • • For the first time pentoses were related with protein accumulation in cyanobacteria.
  • • Xylose and arabinose can be used as carbon sources for Synechococcus and Spirulina.
  • Funding: This research received no external funding.

REFERENCES

  • 1
    Freitas BCB, Esquível MG, Matos RG, et al Nitrogen balancing and xylose addition enhances growth capacity and protein content in Chlorella minutissima cultures. Bioresour Technol. 2016;218:129–33.
  • 2
    Sindhu R, Binod P, Pandey A. Biological pretreatment of lignocellulosic biomass – an overview. Bioresour Technol. 2016;199:76–82.
  • 3
    Seiboth B, Metz B. Fungal arabinan and L-arabinose metabolism. Appl Microbiol Biotechnol. 2011;89:1665–73.
  • 4
    Zheng Y, Yu X, Li T, et al. Induction of D-xylose uptake and expression of NAD(P)H-linked xylose reductase and NADP + -linked xylitol dehydrogenase in the oleaginous microalga Chlorella sorokiniana Biotechnol Biofuels. 2014;7:125.
  • 5
    Freitas BCB, Cassuriaga APA, Morais MG, et al Pentoses and light intensity increase the growth and carbohydrate production and alter the protein profile of Chlorella minutissima Bioresour Technol. 2017;238:248–53.
  • 6
    Freitas BCB, Morais MG, Costa JAV. Chlorella minutissima cultivation with CO2 and pentoses: Effects on kinetic and nutritional parameters. Bioresour Technol. 2017;244:338–44.
  • 7
    Leite GB, Paranjape K, Hallenbeck PC. Breakfast of champions : Fast lipid accumulation by cultures of Chlorella and Scenedesmus induced by xylose. Algal Res. 2016;16:338–48.
  • 8
    Leite GB, Paranjape K, Abdelaziz AEM, et al Utilization of biodiesel-derived glycerol or xylose for increased growth and lipid production by indigenous microalgae. Bioresour Technol. 2015;184:123–30.
  • 9
    Freitas BCB, Brächer EH, de Morais EG, et al. Cultivation of different microalgae with pentose as carbon source and the effects on the carbohydrate content. Environ Technol. 2017;3330:1–9.
  • 10
    Zarrouk C. Contribution à l’étude d’une cyanophycée. Influence de divers facteurs physiques et chimiques sur la croissance et photosynthèse de Spirulina maxima Geitler. University of Paris; 1966.
  • 11
    Costa JAV, Colla LM, Filho PD. Modelling of Spirulina platensis growth in fresh water using response surface methodology. World J Microbiol Biotechnol. 2002;1:603–7.
  • 12
    Somogyi M. Notes on Sugar Determination. J Biol Chem. 1952;195:19–23.
  • 13
    Miller GL. Use of dinitrosalicylic acid for determination of reducing sufar. Anal Chem. 1959;E-31:420–8.
  • 14
    AOAC. Official Methods of Analysis of the Association of Official Analytical Chemists. 17th ed. Maryland; 2000.
  • 15
    Ores J da C, Amarante MCA de, Kalil SJ. Co-production of carbonic anhydrase and phycobiliproteins by Spirulina sp. and Synechococcus nidulans Bioresour Technol. 2016;219:219–27.
  • 16
    Yang S, Liu G, Meng Y, et al. Utilization of xylose as a carbon source for mixotrophic growth of Scenedesmus obliquus Bioresour Technol. 2014;172:180–5.
  • 17
    Chow TJ, Su HY, Tsai TY, et al Using recombinant cyanobacterium (Synechococcus elongatus) with increased carbohydrate productivity as feedstock for bioethanol production via separate hydrolysis and fermentation process. Bioresour Technol. 2015;184:33–41.
  • 18
    Lanlan Z, Lin C, Junfeng W, et al. Attached cultivation for improving the biomass productivity of Spirulina platensis Bioresour Technol. 2015;181:136–42.
  • 19
    Nowicka B, Kruk J. Powered by light: Phototrophy and photosynthesis in prokaryotes and its evolution. Microbiol Res. 2016;186–187:99–118.
  • 20
    Zeng Y, Feng F, Medova H, et al. Functional type 2 photosynthetic reaction centers found in the rare bacterial phylum Gemmatimonadetes. Proc Natl Acad Sci. 2014;111:7795–800.

Publication Dates

  • Publication in this collection
    25 Nov 2019
  • Date of issue
    2019

History

  • Received
    11 Dec 2018
  • Accepted
    08 July 2019
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