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Extended Temperature Optimum of Photosynthetic Reaction Centers in Rhodobacterales

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Extended Temperature Optimum of Photosynthetic Reaction Centers in Rhodobacterales DOI: 10.32615/ps.2019.039 PHOTOSYNTHETICA 57 (2): 361-366, 2019 Extended temperature optimum of photosynthetic reaction centers in Rhodobacterales D. KAFTAN*,**, H. MEDOVÁ*, V. SELYANIN*, K. KOPEJTKA*,**, and M. KOBLÍŽEK*,**,+ Centre Algatech, Institute of Microbiology CAS, CZ-37981 Třeboň, Czech Republic* Faculty of Science, University of South Bohemia in České Budějovice, CZ-37005, Czech Republic** Abstract Temperature is one of the most important physical factors affecting microbial and biochemical processes. We investigated the performance of photosynthetic apparatus of marine photoheterotrophic bacterium Dinoroseobacter shibae under various temperatures. The primary photochemistry and electron transport was measured using variable infra-red fluorometry in the cells grown between 8–35°C. It was found that the photosynthetic electron transport had a broad temperature optimum between 25–50°C. Moreover, the primary charge separation stayed functional even after rising temperature up to 55°C. The same phenomenon was observed also in other phototrophic Rhodobacterales. The psychrotolerant bacterium Roseisalinus antarcticus reached its maximum electron transport rate at 48°C, 30°C above its growth temperature. We propose that the extended temperature stability may be crucial to maintain photosynthetic function under situation when photosynthetic membranes heat up above their ambient temperature due to the heat dissipation of the excess light energy. Additional key words: aerobic anoxygenic phototrophs; Rhodobaca barguzinensis; Roseobacter; variable fluorescence. Introduction inorganic carbon and use light energy as a supplement for their mostly heterotrophic metabolism. Bacterial order Rhodobacterales (Alphaproteobacteria) It has been reported that AAP abundance positively embraces a large group of species differing significantly correlated with chlorophyll concentration, bacterial in their metabolic properties and ecology. A characteristic abundance, and light availability (Koblížek 2015). The feature of Rhodobacterales is the presence of many species seasonal studies conducted in temperate coastal waters performing anoxygenic photosynthesis (Koblížek et al. of the Baltic Sea (Mašín et al. 2006), and the western 2013). These species harvest light using type-2 reaction Mediterranean (Ferrera et al. 2014) also documented a centers (RCs) containing bacteriochlorophyll (BChl) a positive correlation of AAP abundance and temperature. (Selyanin et al. 2016). Phototrophic Rhodobacterales are However, the observed correlations were weak, so the found in many environments including fresh water bodies, effect may have reflected more complex seasonal trends soda lakes, marine waters, sediments, and soils. These rather than the temperature alone. organisms frequently display a large flexibility in their Despite all of their physiological flexibility, photo- oxygen or salinity tolerance. Members of the Rhodobacter trophic Rhodobacterales only flourish within a relatively (Rba.) and Rhodovulum genera represent classical narrow range of temperatures. The majority of cultured examples of purple nonsulfur bacteria which synthesize Rhodobacterales are mesophilic species with growth pigments and perform photosynthesis under anaerobic or optima between 25–35°C. Several species, Roseovarius semiaerobic conditions. On the other hand, there exist many tolerans, Staleya guttiformis, and Roseisalinus (Ris.) marine species belonging to the so called Roseobacter antarcticus, were isolated from the saline Lake Ekho in group, which grow and express their photosynthetic East Antarctica, but none of them are true psychrophiles complexes in the presence of oxygen (Brinkhoff et al. (Labrenz et al. 1999, 2000, 2005). A similar situation has 2008). These aerobic anoxygenic phototrophic (AAP) been documented for the opposite temperature extreme. bacteria are typical photoheterotrophs, they do not fix Despite numerous attempts, no truly thermophilic species Received 31 July 2018, accepted 14 November 2018. +Corresponding author; phone: +420-384340432, e-mail: [email protected] Abbreviations: AAP – aerobic anoxygenic phototrophs; BChl – bacteriochlorophyll; F0 – minimal BChl fluorescence; FM – maximal BChl fluorescence; FV – variable BChl fluorescence; FV/FM – maximal photochemical yield of RC; HPLC – high performance liquid chromatography; OD600 – optical density, turbidity measured at 600 nm; RC – photosynthetic reaction center. Acknowledgements: This research was supported by GAČR project 15-00703S, the Czech Ministry of Education project Algatech Plus (LO1416), and by European Regional Development Fund Project ʻMechanisms and dynamics of macromolecular complexes: from single molecules to cellsʼ (no. CZ.02.1.01/0.0/0.0/15_003/0000441). The authors thank Dr. Mathias Labrenz for providing his strain Roseisalinus antarcticus, Martina Hanusová for laboratory assistance, and Jason Dean for the language correction. The authors declare no competing financial interests. 361 D. KAFTAN et al. (growing above 50°C) have been cultured to date (Madigan surements were performed using a kinetic fluorometer and Jung 2009, Kalashnikov et al. 2014). Most of the FL-3000 (Photon Systems Instruments Ltd., Brno, Czech research on thermostability of bacterial reaction centers Republic) equipped with the ʻSuperheadʼ optical unit has been conducted with mildly thermophilic species populated with an array of blue-green 505 nm Luxeon Thermochromatium tepidum (Nozawa and Madigan 1991, Rebel diodes. The infra-red (BChl) fluorescence signal Kimura et al. 2009). However, this purple sulfur bacterium (λ > 850 nm) was detected using a silicon photodiode (class Gammaproteobacteria) differs dramatically from registering with a 10 MHz resolution. The cells harvested Rhodobacterales regarding its ecology, physiology as well at late exponential phase were diluted 10 times into as phylogeny. fresh medium and dark adapted for half an hour at room In general, temperature has a profound effect on micro- temperature prior to probing their photosynthetic activity. bial growth and activity since it directly affects the rate Cell suspension (2.3 mL) was first cooled down to 10°C and of biochemical reactions. Temperature may also affect then in the dark linearly heated to the selected temperature the metabolic patterns, the nutritional requirements, and over a period of 10 min. Heating period was chosen as a the composition of microbial cells. Low temperatures are minimal time required for inducing a stable half inhibition known to limit respiration and restrict bacterial growth. of the yield of primary photochemistry of the reaction On the other hand, a high temperature may disrupt cellular centers at 70°C (Fig. S1, supplement). After reaching the metabolism and regulation, damage enzymes and affect chosen temperature, the BChl fluorescence was elicited the overall cellular apparatus. by a 140 μs-long square-wave pulse of light with an To learn more about the performance of bacterial intensity of ~ 0.1 mol(photon) m–2 s–1. The yield of primary photosynthetic RCs at various temperatures, we investi- photochemistry was calculated as FV/FM = (FM – F0)/FM. gated the temperature preference of pigment synthesis, Here, F0 is the minimal BChl fluorescence yield at time primary photochemistry, and electron transport in marine 1 μs emitted by the open reaction centers capable of charge AAP bacterium Dinoroseobacter (Drb.) shibae (Biebl et al. separation. The FM is the maximal BChl fluorescence yield 2005). In addition, we also used other photoheterotrophic obtained after 100 μs of illumination that is emitted by Rhodobacterales differing in their temperature preference. the closed reaction centers that have undergone charge The psychrotolerant bacterium Ris. antarcticus EL-88T separation and stabilization of the electron at the quinone was isolated from Antarctic lake Ekho, the haloalkaliphile primary acceptor QA. The fluorescence relaxation following Rhodobaca (Rca.) barguzinensis alga-05 was isolated the maximal BChl fluorescence level FM was detected by from a soda lake in Siberia (Boldareva et al. 2008), 124 logarithmically spaced probing flashlets placed after while the marine bacterium Roseobacter sp. COL2P was the saturating pulse. The normalized BChl fluorescence isolated from Mediterranean coastal waters (Koblížek et decays were fitted with three exponential-decay curves al. 2010). The function of their photosynthetic RCs at by least square numerical fitting. The rate of fluorescence various temperatures was investigated using kinetic BChl relaxation was expressed as a sum of three components fluorometry. f(t) = a1 exp(–k1 t) + a2 exp(–k2 t) + a3 exp(–k3 t), where f(t) is the fluorescence response at timet ; k1, k2, and k3 represent the rate constants of reoxidation of the primary quinone Materials and methods - electron acceptor QA , and a1, a2, and a3 their corresponding Microbial cultures: Drb. shibae DFL-12T, Ris. antarc- amplitude. The individual measurements were conducted ticus EL-88T, and Roseobacter sp. COL2P were grown over a range from 5 to 90°C with 2.5°C increments with a in complex organics seawater media described before fresh sample for each individual measurement (i.e., in total (Koblížek et al. 2010). Rca. barguzinensis alga-05 was of 35 measurements). grown in organic medium designed for haloalkalophic species (Boldareva et al. 2008). The aerobic cultures were Other analyses and statistics: The rate of respiration incubated in 250-mL Erlenmayer flasks with cotton plugs was measured with
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