Differential catalase activity and tolerance to hydrogen peroxide in the filamentous cyanobacteria Nostoc punctiforme ATCC 29113 and Anabaena sp. PCC 7120

doi:10.21203/rs.3.rs-624017/v1

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Differential catalase activity and tolerance to hydrogen peroxide in the filamentous cyanobacteria Nostoc punctiforme ATCC 29113 and Anabaena sp. PCC 7120

https://doi.org/10.21203/rs.3.rs-624017/v1

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Photoautotrophic cyanobacteria often confront hydrogen peroxide (H2O2), a reactive oxygen species potentially toxic to cells when present in sufficiently high concentrations. In this study, H2O2 tolerance ability of filamentous cyanobacteria Nostoc punctiforme ATCC 29133 (Nostoc 29133) and Anabaena sp. PCC 7120 (Anabaena 7120) was investigated. Nostoc 29133 was better able to tolerate H2O2-induced inhibition of chlorophyll a and photosystem II performance, as compared to Anabaena 7120. The intracellular hydroperoxide level (indicator of oxidative status) also did not exhibit as much a rise in Nostoc 29133, as it did in Anabaena 7120 after H2O2 treatment. Accordingly, Nostoc 29133 showed higher intrinsic constitutive catalase activity than Anabaena 7120 indicating that the superior tolerance of Nostoc 29133 stems from its higher ability to decompose H2O2. It is suggested that difference in H2O2 tolerance between closely related filamentous cyanobacteria, as is borne out by this study, may be taken into account for judicious selection and effective use of strains in biotechnology.

General Microbiology

Biotechnology and Bioengineering

Biological Chemistry

Anabaena

Catalase

Cyanobacteria

Hydrogen peroxide

Nostoc

Oxidative stress

Hydrogen peroxide (H₂O₂) is one of several reactive oxygen species (ROS) produced as a by-product of photosynthesis and/or respiratory processes in aerobic organisms (Latifi et al. 2009; Imlay 2013). The oxygen evolving photosynthetic cyanobacteria, major drivers of global carbon and nitrogen cycle and potential sources of biofuels and commodity chemicals, produce H₂O₂ mainly through superoxide dismutase (SOD) catalyzed disproportionation of superoxide radical (O₂^•-), a by-product of photosynthetic electron transport activity (Banerjee et al. 2013; Singh et al. 2014; Kitchener and Grunden 2018). Incomplete oxidation of H₂O at the donor side of photosystem II (PSII) also generates H₂O₂ in cyanobacteria (Pospíšil 2009). A wide variety of naturally occurring stressors such as high light, ultraviolet rays, salinity, herbicides, heavy metals, high and low temperature etc. further increase the intracellular concentration of H₂O₂ in cyanobacteria (Latifi et al. 2009; Chauvat and Chauvat 2015; Mironov et al. 2019). Besides, cyanobacteria may also encounter H₂O₂ sourced from metabolic activities of other organisms or from photo-oxidation of chromophoric dissolved organic matter in their natural environments (Diaz and Plummer 2018; Zinser 2018).

While low-concentration H₂O₂ may function as a second messenger in cell signal transduction pathways, sufficiently high concentrations of H₂O₂ cause oxidative stress leading to loss of membrane integrity, destruction of light-harvesting pigments, impairment of PSII reaction center protein D1 and photosynthetic activity, and ultimately cell death in cyanobacteria (Drábková et al. 2007 a, b; Nishiyama et al. 2011; Mikula et al. 2012; Yang et al. 2018; Piel et al. 2019). It has been suggested that such adverse effects are most often not directly caused by H₂O₂,but rather by the ROS hydroxyl radical (HO^•) formed from interaction of H₂O₂ with free intracellular ferrous iron via Fenton chemistry (Imlay 2013). Hence, cyanobacteria must promptly neutralize H₂O₂ to avoid formation of cell lethal HO^•.

Cyanobacteria possess various antioxidative enzymes such as thiol-specific peroxiredoxins (Prxs) and catalases to neutralize H₂O₂ (Latifi et al. 2009; Banerjee et al. 2013). Whereas, Prxs reduce low concentrations of H₂O₂ (K_M inµM range), catalases efficiently decompose high concentrations of H₂O₂ (K_M inmM range) (Tichy and Vermaas 1999). Comparative genome sequence analysis in cyanobacteria has revealed that unlike Prxs, the distribution of catalases is not uniform; a large number of them (nearly 50 %) lack catalase-encoding gene (Bernroitner et al. 2009). Accordingly, several studies also revealed higher sensitivity to H₂O₂ in some cyanobacteria which lack catalase, such as the unicellular fresh water Microcystis aeruginosa and marine-dwelling Prochlorococcus (Morris et al. 2011; Mikula et al. 2012). Conversely, the ones containing catalase (heme-dependent KatG) like unicellular, non-diazotrophic cyanobacteria Synechocystis sp. PCC 6803 and Synechococcus sp. PCC 7942 have been shown to tolerate high concentrations of H₂O₂ (Tichy and Vermaas 1999; Perelman et al. 2003). On the other hand, many KatG-lacking filamentous diazotrophic cyanobacteria, particularly the species of Anabaena, which possess at least one catalase with manganese as cofactor (Mn-catalase), are reported to lack catalase activity, irrespective of whether they were grown in the presence or absence of H₂O₂ (Bagchi et al. 1991; Bernroitner et al. 2009; Banerjee et al. 2012; Chakravarty et al. 2016; Ballal et al. 2020). Correspondingly, Anabaena sp. PCC 7120 despite possessing two Mn-catalases, was more sensitive to H₂O₂, as compared to Synechocystis sp. PCC 6803 (Pascual et al. 2010). A report also suggests that owing to higher basal level catalase activity Synechococcus sp. PCC 7942 is more tolerant to H₂O₂ than Synechocystis sp. PCC 6803 (Gupta and Ballal 2015). It is presently unclear whether variation in H₂O₂ tolerance also exists among filamentous cyanobacteria. Such information may be important, as this may lead to identification of stress resilient strains to be used in biotechnological applications (Kitchener and Grunden 2018).

In this study, H₂O₂ tolerance ability of Nostocpunctiforme ATCC 29133 (hereafter Nostoc 29133) was evaluated with respect to the reference strain Anabaena sp. PCC 7120 (hereafter Anabaena 7120) to determine possible differences, if any, between these two taxonomically closely related filamentous cyanobacteria. However, unlike Anabaena 7120, Nostoc 29133 has a symbiotic origin and isolated from the cycad Macrozamia (Meeks et al. 2001; Campbell et al. 2008). Nostoc 29133 has previously been shown to adapt to a variety of stresses, including UVA radiation, herbicide methyl viologen and heavy metals (Soule et al. 2009; Moirangthem et al. 2014; Hudek et al. 2017). This cyanobacterium is also considered a potential candidate for production of biofuels and many other high-value compounds (Moraes et al. 2017). The findings presented in this study show that Nostoc 29133 is relatively more tolerant to H₂O₂ than Anabaena 7120 due to its higher intrinsic constitutive H₂O₂ decomposition activity. This suggests that differences in H₂O₂ tolerance may exist even between closely related filamentous cyanobacteria. Further, the unique H₂O₂ stress-tolerant property of Nostoc 29133 is likely to add to its biotechnological value.

Cyanobacterial strains and culture conditions

The batch cultures of Nostoc 29133 (Nostoc punctiforme strain ATCC 29133-S, also known as UCD 153, Campbell et al. 2008) and Anabaena 7120 (Anabaena sp. PCC strain 7120) were grown at 25 °C in BG11-liquid medium, pH 7.5, containing 17.6 mM sodium nitrate buffered with equimolar 4-(2-Hydroxyethyl)-1-piperazine ethane sulphonic acid (HEPES) from stock cultures maintained on slants containing BG11-solid medium with 1.5 % agar (Rippka et al. 1979). The cultures were continuously illuminated with cool fluorescent light (photon fluence rate of 20-23 µmol m^-2 s^-1) during growth period, as described earlier (Moirangthem et al. 2014).

Determination of H₂O₂tolerance

For H₂O₂tolerance assay, the actively growing cultures, 100 ml each of Nostoc 29133 and Anabaena 7120, were pooled separately and washed twice with fresh BG11-medium. Such cultures were inoculated separately in 30 ml of fresh BG11-medium at equal chlorophyll a (Chl a) concentration. The H₂O₂ stock (30 % v/v; Merck, India)was diluted to 10 mM concentration with sterile Milli-Q water and subsequently different volumes of H₂O₂ were added to the cyanobacterial cultures at the start of the experiment to obtain concentrations ranging from 0-0.5 mM H₂O_2, and incubated as described above. Growth was monitored periodically by measuring the concentration of Chl a spectrophotometrically (Cary 60, Agilent, USA) in methanolic extracts of cyanobacterial cultures using absorbance value at 663 nm × 13.43, where 13.43 represents extinction coefficient of Chl a (Mackinney 1941; Moirangthem et al. 2014).

Pulse amplitude modulated (PAM) fluorometry

The maximal efficiency of PSII photochemistry (F_v/F_m), which is a common and quick indicator of photosynthetic performance of cells, was measured in H₂O₂ treated and untreated cultures of both the cyanobacterial species after 15 min of dark adaptation using a Dual-PAM-100 fluorometer (Waltz, Effeltrich, Germany), as described earlier (Moirangthem et al., 2014). The F_v/F_m values were derived from F_v = (F_m-F₀), where F_v represents the variable fluorescence signal, F₀ minimal fluorescence signal of dark adapted cells, and F_m the maximal fluorescence signal after application of a saturating light pulse (Schreiber et al. 1995).

Determination of total intracellular hydroperoxide

The total hydroperoxide levels was measured in cyanobacterial cells after incubation in the presence of different concentrations of H₂O₂ (0-0.5 mM) for one day by a ferrous oxidation/xylenol orange (FOX) assay method as described earlier (DeLong et al. 2002; Moirangthem et al. 2014; Wolff 1994).

Determination of catalase activity

The cultures of Nostoc 29133 and Anabaena 7120 were exposed to increasing concentrations of H₂O₂for a day. Such cells were centrifuged at 2300×g for 5 min, and the cell pellets obtained were washed twice with 36 mM potassium phosphate buffer (pH 7.4). The cell-free extracts were obtained by sonication of the cell pellets in the same buffer added with 1 mM protease inhibitor phenylmethylsulphonyl fluoride (PMSF), as described earlier (Moirangthem et al. 2014). The total protein in cell extracts was measured according to Bradford (1976). 50 µg of total protein was added to 50 mM phosphate buffer (pH 7) and 10 mM H₂O₂ in a final volume of 1 ml. Catalase activity was determined by measuring the disappearance of H₂O₂ at 240 nm using an extinction coefficient of 43.6 M^-1 cm^-1 (Beers and Sizer 1952).

Statistical analysis

All experiments were performed at least three times and the results are presented as mean ± standard deviation. The significant differences (P values less than 0.05) were analyzed by Student’s two-sample t-test (Microsoft word version 10) between control and H₂O₂ treated cyanobacterial cultures.

Nostoc 29133 exhibits higher tolerance to H₂O₂ than Anabaena 7120

Cyanobacteria are often exposed to H₂O₂ generated in surrounding environments (Diaz and Plummer 2018; Zinser 2018). Being a small and neutral molecule, extracellular H₂O₂ can readily cross cell membranes and enter into cells. At high concentrations, H₂O₂ can be highly damaging to cellular growth and metabolism, especially if there is free ferrous iron available in the cell since HO^• radicals will be formed by Fenton chemistry (Latifi et al. 2009; Banerjee et al. 2013; Imlay 2013). In order to reveal the potential differences in H₂O₂ tolerance of filamentous Nostoc 29133 and Anabaena 7120, the active cultures of both cyanobacterial strains were subjected to increasing concentrations of exogenously added H₂O₂ (0.1, 0.25, and 0.5 mM), and Chl a content of cultures was measured for 6 days. This range of H₂O₂ concentration was chosen based on studies in Aphanizomonen ovalisporum, a filamentous cyanobacterium, which fails to survive in the presence of 0.5 mM H₂O₂ (Kaplan-Levy et al. 2015). When incubated with 0.1 mM H₂O₂, Chl a content of Nostoc 29133 (Fig. 1a) and Anabaena 7120 (Fig. 1b) was inhibited more or less to similar extent compared to their respective controls. However, a distinct difference between the two strains was observed with increased doses of H₂O₂. Whereas, 0.25 and 0.5 mM H₂O₂ inhibited Chl a content of Nostoc 29133 by 12 to 20 % compared with untreated control (considered 100 %), similar treatments led to complete inhibition in Anabaena 7120. These results suggest that tolerance to H₂O₂ is higher in Nostoc 29133 compared to in Anabaena 7120, despite the two being taxonomically closely related to each other (order Nostocales) (Rippka et al. 1979). Differences in H₂O₂ tolerance among cyanobacteria have been described earlier, but such comparisons have been mostly between different taxonomical groups, for example, comparisons of Anabaena 7120 and Synechocystis sp. PCC 6803 (Pascual et al. 2010), and of Cylindrospermopsis and Planktothrix (Yang et al. 2018). Therefore, H₂O₂ tolerance seems to be a species dependent feature in cyanobacteria, and may be related to differential accumulation of H₂O₂ and/or HO^•(Drábková et al. 2007 a, b; Yang et al. 2018). This possibility was investigated by measuring the intracellular hydroperoxide concentrations in Nostoc 29133 and Anabaena 7120.

Nostoc 29133 displays lower intracellular hydroperoxide levels than Anabaena 7120

Total intracellular hydroperoxide levels (includes lipid hydroperoxides) was determined in the cultures of Nostoc 29133 and Anabaena 7120 exposed to H₂O₂ for 1 day by FOX assay (Wolff 1994; DeLong et al. 2002). As shown in Fig. 2, incubation with 0.1 mM H₂O₂ barely affected the hydroperoxide levels in either strain relative to their respective controls. However, exposure to higher concentrations of H₂O₂ led to differential increase in hydroperoxide levels; Nostoc 29133 displayed considerably lower levels relative to Anabaena 7120. It is highly likely that relatively lower accumulation of hydroperoxides within cells of Nostoc 29133 protected it from H₂O₂ lethality, as opposed to that in Anabaena 7120. To investigate if the ability to keep a low intracellular hydroperoxide concentration is also shown in a lower damage to the metabolism, the inhibition of PSII activity was measured in Nostoc 29133 and Anabaena 7120.

Nostoc 29133 exhibits lower inhibition of PSII performance than Anabaena 7120

PSII is a major target of H₂O₂ in many cyanobacteria (Drábková et al. 2007 a, b; Nishiyama et al. 2011; Mikula et al. 2012; Yang et al. 2018; Piel et al. 2019). The maximum photochemical efficiency of PSII (F_v/F_m), an indicator of PSII electron transport capacity, is a quick and sensitive parameter to assess PSII performance in cyanobacteria (Schreiber et al. 1995). Thus, F_v/F_m was measured in whole cells of Nostoc 29133 and Anabaena 7120 following 1 day treatment with increasing concentrations of H₂O₂ (Fig. 3). The H₂O₂ treated cultures (0.1 and 0.25 mM) of Nostoc 29133 did not show any appreciable change in F_v/F_m values compared to control cultures, though F_v/F_m was inhibited to a smaller extent in 0.5 mM treated cultures. In Anabaena 7120, treatment with 0.1 mM H₂O₂ resulted in a mild inhibition of F_v/F_m compared with control, however, higher concentrations completely inhibited F_v/F_m. These results suggest lower inhibition of PSII performance in Nostoc 29133 than in Anabaena 7120, which may be an effect of tighter regulation of intracellular hydroperoxide levels in the former thus limiting free H₂O₂ to inhibit the PSII.

Nostoc 29133 possesses higher catalase activity than Anabaena 7120

To probe the underlying reason for differential accumulation of hydroperoxides in Nostoc 29133 and Anabaena 7120, catalase activity was evaluated in the cell extracts of 1 day old H₂O₂-treated and untreated cultures. The antioxidative enzymes such as catalases and Prxs are known to participate in scavenging H₂O₂ in cyanobacteria (Tichy and Vermaas 1999; Perelman et al. 2003; Bernroitner et al. 2009; Latifi et al. 2009; Banerjee et al. 2013). However, unlike catalases, Prxs are susceptible to H₂O₂-mediated overoxidation and inactivation (Pascual et al. 2010). As shown in Fig. 4, catalase activity was nearly 20-fold higher in control cultures of Nostoc 29133 than that in control cultures of Anabaena 7120. While a 1.2-fold increase in catalase activity was observed in Nostoc 29133 after 0.25 mM H₂O₂ treatment, an approximately 3-fold increase in this activity was observed in Anabaena 7120, compared to their respective controls. However, such an increase in catalase activity was clearly not enough to prevent death by H₂O₂ in Anabaena 7120 (Fig. 1b). As opposed to Anabaena 7120, a high intrinsic constitutive catalase activity seems to contribute to prompt and efficient decomposition of H₂O₂ resulting in lower intracellular hydroperoxide levels and higher tolerance to H₂O₂ in Nostoc 29133. This correlation of H₂O₂ tolerance and intrinsic catalase activity has also been demonstrated earlier in a comparative study between Synechococcus PCC 7942 and Synechocystis PCC 6803 (Gupta and Ballal 2015). It should be stressed that several cyanobacteria, including the filamentous forms, lack catalase activity and are sensitive to H₂O₂ (Bagchi et al. 1991; Bernroitner et al. 2009; Morris et al. 2011; Banerjee et al. 2012; Mikula et al. 2012; Yang et al. 2018; Piel et al. 2019). In this context, Nostoc 29133 may be unique, as it possesses catalase activity and a superior ability to tolerate H₂O₂. The findings presented here should pave the way for further in-depth characterization of catalases in this filamentous cyanobacterium and their roles in adaptation to H₂O₂ and other abiotic stress conditions, which presumably generate oxidative stress.

This study highlights differences in H₂O₂ tolerance between two closely related filamentous cyanobacteria Nostoc 29133 and Anabaena 7120. Nostoc 29133 exhibited lower inhibition of chlorophyll a and PSII performance, as compared to Anabaena 7120 in response to exogenous H₂O₂. The higher tolerance of Nostoc 29133 to H₂O₂ was accompanied by a tighter control of intracellular hydroperoxide level supported by higher intrinsic constitutive catalase activity, in contrast to that in Anabaena 7120. H₂O₂ stress tolerant photoautotroph like Nostoc 29133 is likely to be an important biotechnological resource, and may be exploited as a potential source of valuable antioxidant catalase.

Acknowledgements

LS acknowledge the financial support from Mizoram University in the form of fellowship. KS and PL acknowledge the financial support by the Swedish Energy Agency. JB is grateful to Department of Science and Technology (FIST), and Department of Biotechnology, Government of India, for Advance State Biotech hub research facility.

Funding: This research did not receive any specific grant from funding agencies.

Competing interests: The authors state that there is no conflict of interest.

Availability of data and material: Not applicable

Code availability: Not applicable

Authors’ contributions: JB and LS conceived and designed the study. LS performed all the experiments. JB and LS interpreted the results. All the authors contributed to the writing of this manuscript. The final version of the manuscript was read and approved by all the authors.

Ethics approval: Not applicable

Consent to participate: Not applicable

Consent for publication: Not applicable

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Differential catalase activity and tolerance to hydrogen peroxide in the filamentous cyanobacteria Nostoc punctiforme ATCC 29113 and Anabaena sp. PCC 7120

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