Abstract
This is the comparative investigation of the composition of phototrophic microbial mats developing in sulfide-rich saline Chokrak springs with outflow at the shore of the hypersaline lake Chokrak by means of next-generation sequencing. The springs are characterized by low temperature (~ 15 °C), near-neutral pH (6.7–8.5), and high-sulfide content. In the species composition the benthic microbial communities of Chokrak springs are similar to microbial mats of marine supralittoral and lagoons. Our results showed that salinity limitation had a significant effect on the species composition of benthic microbial communities developing at the outflow of the Chokrak springs. Predominant oxygenic phototrophs belonged to the genera Phormidium, Lyngbya, Leptolyngbya, Geitlerinema, and Arthrospira. Anoxygenic phototrophic bacteria were represented by halophilic green sulfur bacteria Prosthecochloris spp., halotolerant Chlorobaculum sp., as well as marine and extremely halophilic purple bacteria Roseospira, Rhodovibrio, and Halochromatium. Monoculture of a new species of halotolerant anoxygenic filamentous phototrophic bacteria was isolated.
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References
Albov SV (1973) On geochemical situation ih the Kerch–Taman region and neighbouring areas. In: Reports of the Academy of Sciences of the USSR. V. 208. Nauka, Moscow, pp 184–187
Alexander B, Andersen J, Cox R, Imhoff J (2002) Phylogeny of green sulfur bacteria on the basis of gene sequences of 16S rRNA and of the Fenna-Matthews-Olson protein. Arch Microbiol 178:131–140. https://doi.org/10.1007/s00203-002-0432-4
Baas-Becking LGM (1925) Studies on the sulphur bacteria. Ann Bot 39:613–650. https://doi.org/10.1093/oxfordjournals.aob.a089968
Bachar A, Omoregie E, De Wit R, Jonkers HM (2007) Diversity and function of Chloroflexus-like bacteria in a hypersaline microbial mat: phylogenetic characterization and impact on aerobic respiration. Appl Environ Microbiol 73:3975–3983. https://doi.org/10.1128/AEM.02532-06
Boldareva EN, Moskalenko AA, Makhneva ZK et al. (2009) Rubribacterium polymorphum gen. nov., sp. nov., a novel alkaliphilic nonsulfur purple bacterium from an Eastern Siberian soda lake. Microbiology 78:732–740. https://doi.org/10.1134/S0026261709060101
Bryantseva IA, Gaisin VA, Gorlenko VM (2015) Rhodobaculum claviforme gen. nov., sp. nov., a new alkaliphilic nonsulfur purple bacterium. Microbiology 84:247–255. https://doi.org/10.1134/S0026261715020022
Burganskaya EI, Bryantseva IA, Gaisin VA et al. (2018) Benthic phototrophic community from Kiran soda lake, south-eastern Siberia. Extremophiles 22:211–220. https://doi.org/10.1007/s00792-017-0989-0
Caporaso JG, Kuczynski J, Stombaugh J et al. (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336. https://doi.org/10.1038/nmeth.f.303
Cohen Y, Padan E, Shilo M (1975) Sulfide-dependent anoxygenic photosynthesis in the cyanobacterium Oscillatoria limnetica. Nature 257:489–492. https://doi.org/10.1038/257489a0
Cohen Y, Jorgensen BB, Revsbech NP, Poplawski R (1986) Adaptation to hydrogen sulfide of oxygenic and anoxygenic photosynthesis among cyanobacteria. Appl Environ Microbiol 51:398–407
Csotonyi JT, Swiderski J, Stackebrandt E, Yurkov VV (2008) Novel halophilic aerobic anoxygenic phototrophs from a Canadian hypersaline spring system. Extremophiles 12:529–539. https://doi.org/10.1007/s00792-008-0156-8
de Wit R, van Gemerden H (1987) Oxidation of sulfide to thiosulfate by Microcoleus chtonoplastes. FEMS Microbiol Lett 45:7–13. https://doi.org/10.1016/0378-1097(87)90036-X
Dorador C, Vila I, Witzel K-P, Imhoff JF (2013) Bacterial and archaeal diversity in high altitude wetlands of the Chilean Altiplano. Fundam Appl Limnol/Arch Hydrobiol 182:135–159. https://doi.org/10.1127/1863-9135/2013/0393
Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26:2460–2461. https://doi.org/10.1093/bioinformatics/btq461
Edgar RC, Haas BJ, Clemente JC et al. (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27:2194–2200. https://doi.org/10.1093/bioinformatics/btr381
Elshahed MS, Senko JM, Najar FZ et al. (2003) Bacterial diversity and sulfur cycling in a mesophilic sulfide-rich spring. Appl Environ Microbiol 69:5609–5621. https://doi.org/10.1128/AEM.69.9.5609-5621.2003
Farías ME, Contreras M, Rasuk MC et al. (2014) Characterization of bacterial diversity associated with microbial mats, gypsum evaporites and carbonate microbialites in thalassic wetlands: Tebenquiche and La Brava, Salar de Atacama, Chile. Extremophiles 18:311–329. https://doi.org/10.1007/s00792-013-0617-6
Fernández-Gómez B, Richter M, Schüler M et al. (2013) Ecology of marine bacteroidetes: a comparative genomics approach. ISME J 7:1026–1037. https://doi.org/10.1038/ismej.2012.169
Fomichev MM (1948) Chokrak sulfide-reach springs. In: USSR PH of the A of S of the (ed) Laboratory of Hydrogeological Problems’ materials. V. 1. Moscow, pp 221–232
Gorlenko V, Puchkov A, Demchev V (1985) Photosynthesizing microorganisms of the Supralittoral baths of the White Sea. Biol Sci 5:66–72
Gorlenko VM (1988) Ecological Niches of Green Sulfur and Gliding Bacteria. In: Olson JM, Ormerod JG, Amesz J et al. (eds) Green Photosynthetic Bacteria. Plenum Press, New York, pp 257–268
Grouzdev DS, Rysina MS, Bryantseva IA et al. (2018) Draft genome sequences of `Candidatus Chloroploca asiatica’ and ‘Candidatus Viridilinea mediisalina’, candidate representatives of the Chloroflexales order: phylogenetic and taxonomic implications. Stand Genomic Sci 13:24. https://doi.org/10.1186/s40793-018-0329-8
Grouzdev DS, Burganskaya EI, Krutkina MS et al. (2019) Genome sequence of “Candidatus Viridilinea halotolerans” chok-6, isolated from a saline sulfide-rich spring. Microbiol Resour Announc 8:1–2. https://doi.org/10.1128/MRA.01614-18
Hiraishi A, Ueda Y (1994) Intrageneric structure of the genus Rhodobacter: Transfer of Rhodobacter sulfidophilus and related marine species to the genus Rhodovulum gen. nov. Int J Syst Bacteriol 44:15–23. https://doi.org/10.1099/00207713-44-1-15
Hoehler TM, Bebout BM, Des Marais DJ (2001) The role of microbial mats in the production of reduced gases on the early Earth. Nature 412:324–327. https://doi.org/10.1038/35085554
Imhoff JF (2001) True marine and halophilic anoxygenic phototrophic bacteria. Arch Microbiol 176:243–254. https://doi.org/10.1007/s002030100326
Imhoff JF (2017) Anoxygenic phototrophic bacteria from extreme environments. In: Hallenbeck PC (ed) Modern topics in the phototrophic prokaryotes. Springer International Publishing, Cham, pp 427–480
Imhoff JF, Sueling J, Petri R (1998) Phylogenetic relationships among the Chromatiaceae, their taxonomic reclassification and description of the new genera Allochromatium, Halochromatium, Isochromatium, Marichromatium, Thiococcus, Thiohalocapsa and Thermochromatium. Int J Syst Bacteriol 48:1129–1143
Klappenbach JA, Pierson BK (2004) Phylogenetic and physiological characterization of a filamentous anoxygenic photoautotrophic bacterium ‘Candidatus Chlorothrix halophila’ gen. nov., sp. nov., recovered from hypersaline microbial mats. Arch Microbiol doi. https://doi.org/10.1007/s00203-003-0615-7
Klatt JM, Haas S, Yilmaz P et al. (2015) Hydrogen sulfide can inhibit and enhance oxygenic photosynthesis in a cyanobacterium from sulfidic springs. Environ Microbiol 17:3301–3313. https://doi.org/10.1111/1462-2920.12791
Klyukin A, Korzhenevsky V (2004) Crimean pryazovia: local history guide. Business-Inform, Simferopol
Komárek J, Anagnostidis K (2005) Cyanoprokaryota 2. teil oscillatoriales. Elsevier, Heidelberg
Kompantseva EI, Puchkova NN, Gorlenko VM, Savvichev AS (1989) Phototrophic microorganisms in cold saline water springs with high content of hydrogen sulfide. Microbiology 58:127–132
Lane DJ (1991) 16S/23S rRNA sequencing. In: Stackebrandt E, Goodfellow M (eds) Nucleic acid techniques in bacterial systematics. Wiley, New York, pp 115–175
Ley RE, Harris JK, Wilcox J et al (2006) Unexpected Diversity and Complexity of the Guerrero Negro Hypersaline Microbial Mat. Appl Environ Microbiol 72:3685–3695. https://doi.org/10.1128/AEM.72.5.3685-3695.2006
Martínez-Alonso M, Bleijswijk J, Gaju N, Muyzer G (2005) Diversity of anoxygenic phototrophic sulfur bacteria in the microbial mats of the Ebro Delta: a combined morphological and molecular approach. FEMS Microbiol Ecol 52:339–350. https://doi.org/10.1016/j.femsec.2004.11.021
Milford AD, Achenbach LA, Jung DO, Madigan MT (2000) Rhodobaca bogoriensis gen. nov. and sp. nov., an alkaliphilic purple nonsulfur bacterium from African Rift Valley soda lakes. Arch Microbiol 174:18–27. https://doi.org/10.1007/s002030000166
Miller SR, Miller SR, Bebout BM, Bebout BM (2004) Variation in Sul de tolerance of photosystem II in phylogenetically diverse cyanobacteria from sul dic habitats. Society 70:736–744. https://doi.org/10.1128/AEM.70.2.736
Nübel U, Bateson MM, Madigan MT et al. (2001) Diversity and distribution in hypersaline microbial mats of bacteria related to Chloroflexus spp. Appl Environ Microbiol 67:4365–4371. https://doi.org/10.1128/AEM.67.9.4365-4371.2001
Pfennig N, Lippert KD (1966) Über das vitamin B12-bedürfnis phototropher Schwefelbakterien. Arch Microbiol 55:245–256. https://doi.org/10.1007/BF00410246
Pierson BK, Valdez D, Larsen M et al. (1994) Chloroflexus-like organisms from marine and hypersaline environments: distribution and diversity. Photosynth Res 41:35–52
Sidorenko AV (ed) (1970) Hydrogeology of the USSR. Volume VIII. Crimea. Nedra, Moscow
Stolz JF (1990) Distribution of phototrophic microbes in the flat laminated microbial mat at Laguna Figueroa, Baja California, Mexico. Biosystems 23:345–357. https://doi.org/10.1016/0303-2647(90)90016-T
Tamura K, Stecher G, Peterson D et al. (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729. https://doi.org/10.1093/molbev/mst197
Wang Q, Garrity GM, Tiedje JM, Cole JR (2007) Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73:5261–5267. https://doi.org/10.1128/AEM.00062-07
Whitton BA (ed) (2012) Ecology of cyanobacteria II. Springer Netherlands, Dordrecht
Wong H, Ahmed-Cox A, Burns B (2016) Molecular ecology of hypersaline microbial mats: current insights and new directions. Microorganisms 4:6. https://doi.org/10.3390/microorganisms4010006
Ben Hania W, Joseph M, Bunk B et al (2017) Characterization of the first cultured representative of a Bacteroidetes clade specialized on the scavenging of cyanobacteria. Environ Microbiol 19:1134–1148. https://doi.org/10.1111/1462-2920.13639
Acknowledgements
The authors are grateful to Samylina O.S. from Winogradsky Institute of Microbiology, Research Center of Biotechnology of the Russian Academy of Sciences for her help in identification of cyanobacteria. This work was financially supported by the Presidium of the Russian Academy of Sciences via the program “Evolution of the Organic World and Planet-Scale Processes” (Subprogram 2), by the Russian Foundation for Basic Research (Project no. 19-04-00423) and the Ministry of Science and Higher Education of the Russian Federation. DNA sequencing was partially performed using the equipment of the Collective Use Center “Bioengineering” of the Federal Research Center of Biotechnology.
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Burganskaya, E.I., Bryantseva, I.A., Krutkina, M.S. et al. Bacterial communities of the microbial mats of Chokrak sulfide springs. Arch Microbiol 201, 795–805 (2019). https://doi.org/10.1007/s00203-019-01648-6
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DOI: https://doi.org/10.1007/s00203-019-01648-6