Diversity dynamics of aerobic anoxygenic phototrophic bacteria in a freshwater lake

. 2023 Feb ; 15 (1) : 60-71. [epub] 20221212

Jazyk angličtina Země Spojené státy americké Médium print-electronic

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid36507772

Aerobic anoxygenic photoheterotrophic (AAP) bacteria represent a functional group of prokaryotic organisms that harvests light energy using bacteriochlorophyll-containing photosynthetic reaction centers. They represent an active and rapidly growing component of freshwater bacterioplankton, with the highest numbers observed usually in summer. Species diversity of freshwater AAP bacteria has been studied before in lakes, but its seasonal dynamics remain unknown. In this report, we analysed temporal changes in the composition of the phototrophic community in an oligo-mesotrophic freshwater lake using amplicon sequencing of the pufM marker gene. The AAP community was dominated by phototrophic Gammaproteobacteria and Alphaproteobacteria, with smaller contribution of phototrophic Chloroflexota and Gemmatimonadota. Phototrophic Eremiobacteriota or members of Myxococcota were not detected. Interestingly, some AAP taxa, such as Limnohabitans, Rhodoferax, Rhodobacterales or Rhizobiales, were permanently present over the sampling period, while others, such as Sphingomonadales, Rhodospirillales or Caulobacterales appeared only transiently. The environmental factors that best explain the seasonal changes in AAP community were temperature, concentrations of oxygen and dissolved organic matter.

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Anderson, M.J. , Gorley, R.N. & Clarke, K.R. (2008) PERMANOVA+ for PRIMER: guide to software and statistical methods. In: Plymouth. UK, PRIMER‐E. pp. 1–214.

Anderson, M.J. & Legendre, P. (1999) An empirical comparison of permutation methods for tests of partial regression coefficients in a linear model. Journal of Statistical Computation and Simulation, 62, 271–303.

Andrei, A.‐Ş. , Salcher, M.M. , Mehrshad, M. , Rychtecký, P. , Znachor, P. & Ghai, R. (2019) Niche‐directed evolution modulates genome architecture in freshwater Planctomycetes. The ISME Journal, 13, 1056–1071. PubMed PMC

Cabello‐Yeves, P.J. , Haro‐Moreno, J.M. , Martin‐Cuadrado, A.‐B. , Ghai, R. , Picazo, A. , Camacho, A. et al. (2017) Novel Synechococcus genomes reconstructed from freshwater reservoirs. Frontiers in Microbiology, 8, 1151. PubMed PMC

Caliz, J. & Casamayor, E.O. (2014) Environmental controls and composition of anoxygenic photoheterotrophs in ultraoligotrophic high‐altitude lakes (Central Pyrenees). Environmental Microbiology Reports, 6, 145–151. PubMed

Callahan, B.J. , McMurdie, P.J. , Rosen, M.J. , Han, A.W. , Johnson, A.J.A. & Holmes, S.P. (2016) DADA2: high‐resolution sample inference from Illumina amplicon data. Nature Methods, 13, 581–583. PubMed PMC

Cepáková, Z. , Hrouzek, P. , Žišková, E. , Nuyanzina‐Boldareva, E. , Šorf, M. , Kozlíková‐Zapomělová, E. et al. (2016) High turnover rates of aerobic anoxygenic phototrophs in European freshwater lakes. Environmental Microbiology, 18, 5063–5071. PubMed

Coleman, A.W. (1980) Enhanced detection of bacteria in natural environments by fluorochrome staining of DNA1. Limnology and Oceanography, 25, 948–951.

Cottrell, M.T. , Mannino, A. & Kirchman, D.L. (2006) Aerobic Anoxygenic phototrophic bacteria in the mid‐Atlantic bight and the North Pacific gyre. Applied and Environmental Microbiology, 72, 557–564. PubMed PMC

Cram, J.A. , Xia, L.C. , Needham, D.M. , Sachdeva, R. , Sun, F. & Fuhrman, J.A. (2015) Cross‐depth analysis of marine bacterial networks suggests downward propagation of temporal changes. The ISME Journal, 9, 2573–2586. PubMed PMC

Čuperová, Z. , Holzer, E. , Salka, I. , Sommarug, R. & Koblížek, M. (2013) Temporal changes and altitudinal distribution of aerobic anoxygenic phototrophs in mountain lakes. Applied and Environmental Microbiology, 79, 6439–6446. PubMed PMC

Dodds, W.K. & Whiles, M.R. (2020) Freshwater ecology: concepts and environmental applications of limnology. In: Chapter 9 ‐ Microbes and plants, Third edition. Academic Press, Elsevier, London, UK, pp. 211–249.

Fauteux, L. , Cottrell, M.T. , Kirchman, D.L. , Borrego, C.M. , Garcia‐Chaves, M.C. & del Giorgio, P.A. (2015) Patterns in abundance, cell size and pigment content of aerobic Anoxygenic phototrophic bacteria along environmental gradients in Northern Lakes. PLoS One, 10, 1–17. PubMed PMC

Fecskeová, L. , Piwosz, K. , Hanusová, M. , Nedoma, J. , Znachor, P. & Koblížek, M. (2019) Diel changes and diversity of pufM expression in freshwater communities of anoxygenic phototrophic bacteria. Scientific Reports, 9, 18766. PubMed PMC

Ferrera, I. , Sarmento, H. , Priscu, J.C. , Chiuchiolo, A. , González, J.M. & Grossart, H.‐P. (2017) Diversity and distribution of freshwater aerobic Anoxygenic phototrophic bacteria across a wide latitudinal gradient. Frontiers in Microbiology, 8, 175. PubMed PMC

Galachyants, A.D. , Krasnopeev, A.Y. , Podlesnaya, G.V. , Potapov, S.A. , Sukhanova, E.V. , Tikhonova, I.V. et al. (2021) Diversity of aerobic Anoxygenic phototrophs and rhodopsin‐containing bacteria in the surface microlayer, water column and Epilithic biofilms of Lake Baikal. Microorganisms, 9, 842. PubMed PMC

Garcia‐Chaves, M.C. , Cottrell, M.T. , Kirchman, D.L. , Ruiz‐González, C. & Del Giorgio, P.A. (2016) Single‐cell activity of freshwater aerobic anoxygenic phototrophic bacteria and their contribution to biomass production. The ISME Journal, 10, 1579–1588. PubMed PMC

Gołębiewski, M. , Całkiewicz, J. , Creer, S. & Piwosz, K. (2017) Tideless estuaries in brackish seas as possible freshwater‐marine transition zones for bacteria: the case study of the Vistula river estuary. Environmental Microbiology Reports, 9, 129–143. PubMed

Hahn, M.W. , Scheuerl, T. , Jezberová, J. , Koll, U. , Jezbera, J. , Šimek, K. et al. (2012) The passive yet successful way of planktonic life: genomic and experimental analysis of the ecology of a free‐living Polynucleobacter population. PLoS One, 7, e32772. PubMed PMC

Harashima, K. , Shiba, T. , Totsuka, T. , Simidu, U. & Taga, N. (1978) Occurrence of bacteriochlorophyll a in a strain of an aerobic heterotrophic bacterium. Agricultural and Biological Chemistry, 42, 1627–1628.

Hauruseu, D. & Koblížek, M. (2012) Influence of light on carbon utilization in aerobic Anoxygenic phototrophs. Applied and Environmental Microbiology, 78, 7414–7419. PubMed PMC

Imhoff, J.F. , Rahn, T. , Künzel, S. & Neulinger, S.C. (2019) Phylogeny of Anoxygenic photosynthesis based on sequences of photosynthetic reaction center proteins and a key enzyme in bacteriochlorophyll biosynthesis, the Chlorophyllide reductase. Microorganisms, 7, 576. PubMed PMC

Jezberová, J. , Jezbera, J. , Znachor, P. , Nedoma, J. , Kasalický, V. & Šimek, K. (2017) The Limnohabitans genus harbors Generalistic and opportunistic subtypes: evidence from spatiotemporal succession in a canyon‐shaped reservoir. Applied and Environmental Microbiology, 83, e01530–e01517. PubMed PMC

Kalyaanamoorthy, S. , Minh, B.Q. , Wong, T.K.F. , von Haeseler, A. & Jermiin, L.S. (2017) ModelFinder: fast model selection for accurate phylogenetic estimates. Nature Methods, 14, 587–589. PubMed PMC

Kasalický, V. , Zeng, Y. , Piwosz, K. , Šimek, K. , Kratochvilová, H. & Koblížek, M. (2018) Aerobic anoxygenic photosynthesis is commonly present within the genus Limnohabitans. Applied and Environmental Microbiology, 84, 6–17. PubMed PMC

Kirchman, D.L. & Hanson, T.E. (2013) Bioenergetics of photoheterotrophic bacteria in the oceans. Environmental Microbiology Reports, 5, 188–199. PubMed

Klindworth, A. , Pruesse, E. , Schweer, T. , Peplies, J. , Quast, C. , Horn, M. et al. (2013) Evaluation of general 16 S ribosomal RNA gene PCR primers for classical and next‐generation sequencing‐based diversity studies. Nucleic Acids Research, 41, e1. PubMed PMC

Koblížek, M. (2015) Ecology of aerobic anoxygenic phototrophs in aquatic environments. FEMS Microbiology Reviews, 39, 854–870. PubMed

Koblížek, M. , Stoń‐Egiert, J. , Sagan, S. & Kolber, Z.S. (2005) Diel changes in bacteriochlorophyll a concentration suggest rapid bacterioplankton cycling in the Baltic Sea. FEMS Microbiology Ecology, 51, 353–361. PubMed

Kolářová, E. , Medová, H. , Piwosz, K. & Koblížek, M. (2019) Seasonal dynamics of aerobic anoxygenic phototrophs in freshwater lake Vlkov. Folia Microbiologia (Praha), 64, 705–710. PubMed

Kopáček, J. & Hejzlar, J. (1993) Semi‐micro determination of Total phosphorus in fresh waters with Perchloric acid digestion. International Journal of Environmental Analytical Chemistry, 53, 173–183.

Kopáček, J. & Procházková, L. (1993) Semi‐micro determination of ammonia in water by the rubazoic acid method. International Journal of Environmental Analytical Chemistry, 53, 243–248.

Kopejtka, K. , Tomasch, J. , Zeng, Y. , Tichý, M. , Sorokin, D.Y. & Koblížek, M. (2017) Genomic analysis of the evolution of Phototrophy among Haloalkaliphilic Rhodobacterales. Genome Biology and Evolution, 9, 1950–1962. PubMed PMC

Kopejtka, K. , Zeng, Y. , Kaftan, D. , Selyanin, V. , Gardian, Z. , Tomasch, J. et al. (2021) Characterization of the aerobic Anoxygenic phototrophic bacterium Sphingomonas sp. AAP5. Microorganisms, 9, 768. PubMed PMC

Lanyi, J.K. (2004) Bacteriorhodopsin. Annual Review of Physiology, 66, 665–688. PubMed

Larkin, M.A. , Blackshields, G. , Brown, N.P. , Chenna, R. , McGettigan, P.A. , McWilliam, H. et al. (2007) Clustal W and Clustal X version 2.0. Bioinformatics, 23, 2947–2948. PubMed

Legendre, P. & Andersson, M.J. (1999) Distance‐based redundancy analysis: testing multispecies responses in multifactorial ecological experiments. Ecological Monographs, 69, 512–524.

Letunic, I. & Bork, P. (2021) Interactive tree of life (iTOL) v5: an online tool for phylogenetic tree display and annotation. Nucleic Acids Research, 49, W293–W296. PubMed PMC

Lew, S. , Koblížek, M. , Lew, M. , Medová, H. , Glińska‐Lewczuk, K. & Owsianny, P.M. (2015) Seasonal changes of microbial communities in two shallow peat bog lakes. Folia Microbiologia (Praha), 60, 165–175. PubMed

Martin, M. (2011) Cutadapt removes adapter sequences from high‐throughput sequencing reads. EMBnet.journal, 17, 10.

Martinez, J.N. , Kawai, S. , Saini, M.K. , Tank, M. , Hanada, S. & Thiel, V. (2020) Draft genome sequence of a filamentous Anoxygenic phototrophic bacterium, “Candidatus Roseilinea sp. strain NK_OTU‐006,” recovered from metagenomic data of a hot spring microbial mat. Microbiology Resource Announcements, 9, e01104–e01120. PubMed PMC

Martinez‐Garcia, M. , Swan, B.K. , Poulton, N.J. , Gomez, M.L. , Masland, D. , Sieracki, M.E. et al. (2012) High‐throughput single‐cell sequencing identifies photoheterotrophs and chemoautotrophs in freshwater bacterioplankton. The ISME Journal, 6, 113–123. PubMed PMC

Mašín, M. , Čuperová, Z. , Hojerová, E. , Salka, I. , Grossart, H. & Koblížek, M. (2012) Distribution of aerobic anoxygenic phototrophic bacteria in glacial lakes of northern Europe. Aquatic Microbial Ecology, 66, 77–86.

Mašín, M. , Nedoma, J. , Pechar, L. & Koblížek, M. (2008) Distribution of aerobic anoxygenic phototrophs in temperate freshwater systems. Environmental Microbiology, 10, 1988–1996. PubMed

McMurdie, P.J. & Holmes, S. (2013) Phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLoS One, 8, e61217. PubMed PMC

Mehrshad, M. , Salcher, M.M. , Okazaki, Y. , Nakano, S.I. , Šimek, K. , Andrei, A.S. et al. (2018) Hidden in plain sight ‐ highly abundant and diverse planktonic freshwater Chloroflexi 06 biological sciences 0602 ecology 05 environmental sciences 0502 environmental science and management. Microbiome, 6, 176. PubMed PMC

Mendler, K. , Chen, H. , Parks, D.H. , Lobb, B. , Hug, L.A. & Doxey, A.C. (2019) AnnoTree: visualization and exploration of a functionally annotated microbial tree of life. Nucleic Acids Research, 47, 4442–4448. PubMed PMC

Morrison, J.M. , Baker, K.D. , Zamor, R.M. , Nikolai, S. , Elshahed, M.S. & Youssef, N.H. (2017) Spatiotemporal analysis of microbial community dynamics during seasonal stratification events in a freshwater Lake (grand lake, OK, USA). PLoS One, 12, e0177488. PubMed PMC

Mujakić, I. , Andrei, A.‐Ş. , Shabarova, T. , Fecskeová, L.K. , Salcher, M.M. , Piwosz, K. et al. (2021) Common presence of phototrophic Gemmatimonadota in temperate Freshwater Lakes. mSystems, 6, 1241–1220. PubMed PMC

Murphy, J. & Riley, J.P. (1962) A modified single solution method for the determination of phosphate in natural waters. Analytica Chimica Acta, 27, 31–36.

Nakahara, N. , Nobu, M.K. , Takaki, Y. , Miyazaki, M. , Tasumi, E. , Sakai, S. et al. (2019) Aggregatilinea lenta gen. Nov., sp. nov., a slow‐growing, facultatively anaerobic bacterium isolated from subseafloor sediment, and proposal of the new order aggregatilineales Ord. Nov. within the class anaerolineae of the phylum chloroflexi. International Journal of Systematic and Evolutionary Microbiology, 69, 1185–1194. PubMed

Niño‐García, J.P. , Ruiz‐González, C. & Del Giorgio, P.A. (2016) Interactions between hydrology and water chemistry shape bacterioplankton biogeography across boreal freshwater networks. The ISME Journal, 10, 1755–1766. PubMed PMC

Parks, D.H. , Chuvochina, M. , Waite, D.W. , Rinke, C. , Skarshewski, A. , Chaumeil, P.A. et al. (2018) A standardized bacterial taxonomy based on genome phylogeny substantially revises the tree of life. Nature Biotechnology, 36, 996–1004. PubMed

Parks, D.H. , Rinke, C. , Chuvochina, M. , Chaumeil, P.‐A. , Woodcroft, B.J. , Evans, P.N. et al. (2017) Recovery of nearly 8000 metagenome‐assembled genomes substantially expands the tree of life. Nature Microbiology, 2, 1533–1542. PubMed

Piwosz, K. , Kaftan, D. , Dean, J. , Šetlík, J. & Koblížek, M. (2018) Nonlinear effect of irradiance on photoheterotrophic activity and growth of the aerobic anoxygenic phototrophic bacterium Dinoroseobacter shibae. Environmental Microbiology, 20, 724–733. PubMed

Piwosz, K. , Villena‐Alemany, C. & Mujakić, I. (2022) Photoheterotrophy by aerobic anoxygenic bacteria modulates carbon fluxes in a freshwater lake. The ISME Journal, 16, 1046–1054. PubMed PMC

Piwosz, K. , Vrdoljak Tomaš, A. , Thijs, F. , Gonzalez Olalla, J.M. , Šantić, D. , McKay, L. et al. (2020) Light and primary production shape bacterial activity and community composition of aerobic Anoxygenic phototrophic bacteria in a microcosm experiment. mSphere, 5, 1–17. PubMed PMC

Procházková, L. (1959) Bestimmung der Nitrate im Wasser. Fresenius' Zeitschrift für Analytische Chemie, 167, 254–260.

Ruiz‐González, C. , Garcia‐Chaves, M.C. , Ferrera, I. , Niño‐García, J.P. & Giorgio, P.A. (2020) Taxonomic differences shape the responses of freshwater aerobic anoxygenic phototrophic bacterial communities to light and predation. Molecular Ecology, 29, 1267–1283. PubMed

Ruiz‐González, C. , Proia, L. , Ferrera, I. , Gasol, J.M. & Sabater, S. (2013) Effects of large river dam regulation on bacterioplankton community structure. FEMS Microbiology Ecology, 84, 316–331. PubMed

Salka, I. , Čuperová, Z. , Mašín, M. , Koblížek, M. & Grossart, H.‐P. (2011) Rhodoferax‐related pufM gene cluster dominates the aerobic anoxygenic phototrophic communities in German freshwater lakes. Environmental Microbiology, 13, 2865–2875. PubMed

Shade, A. , Read, J.S. , Youngblut, N.D. , Fierer, N. , Knight, R. , Kratz, T.K. et al. (2012) Lake microbial communities are resilient after a whole‐ecosystem disturbance. The ISME Journal, 6, 2153–2167. PubMed PMC

Šimek, K. , Horňák, K. , Jezbera, J. , MaŠín, M. , Nedoma, J. , Gasol, J.M. et al. (2005) Influence of top‐down and bottom‐up manipulations on the R‐BT065 subcluster of β‐Proteobacteria, an abundant Group in Bacterioplankton of a freshwater reservoir. Applied and Environmental Microbiology, 71, 2381–2390. PubMed PMC

Spudich, J.L. & Luecke, H. (2002) Sensory rhodopsin II: functional insights from structure. Current Opinion in Structural Biology, 12, 540–546. PubMed

Trifinopoulos, J. , Nguyen, L.‐T. , von Haeseler, A. & Minh, B.Q. (2016) W‐IQ‐TREE: a fast online phylogenetic tool for maximum likelihood analysis. Nucleic Acids Research, 44, W232–W235. PubMed PMC

Tsementzi, D. , Rodriguez‐R, L.M. , Ruiz‐Perez, C.A. , Meziti, A. , Hatt, J.K. & Konstantinidis, K.T. (2019) Ecogenomic characterization of widespread, closely‐related SAR11 clades of the freshwater genus “Candidatus Fonsibacter” and proposal of Ca. Fonsibacter lacus sp. nov. Systematic and Applied Microbiology, 42, 495–505. PubMed

Verpoorter, C. , Kutser, T. , Seekell, D.A. & Tranvik, L.J. (2014) A global inventory of lakes based on high‐resolution satellite imagery. Geophysical Research Letters, 41, 6396–6402.

Ward, L.M. , Cardona, T. & Holland‐Moritz, H. (2019) Evolutionary implications of anoxygenic phototrophy in the bacterial phylum Candidatus Eremiobacterota (WPS‐2). Frontiers in Microbiology, 10, 1–12. PubMed PMC

Wickham, H. (2009) ggplot2: elegant graphics for data analysis.

Woyke, T. , Doud, D.F.R. & Schulz, F. (2017) The trajectory of microbial single‐cell sequencing. Nature Methods, 14, 1045–1054. PubMed

Yamada, T. & Sekiguchi, Y. (2009) Cultivation of uncultured Chloroflexi subphyla: significance and ecophysiology of formerly uncultured Chloroflexi “subphylum i” with natural and biotechnological relevance. Microbes and Environments, 24, 205–216. PubMed

Yamada, T. , Sekiguchi, Y. , Hanada, S. , Imachi, H. , Ohashi, A. , Harada, H. et al. (2006) Anaerolinea thermolimosa sp. nov., Levilinea saccharolytica gen. Nov., sp. nov. and Leptolinea tardivitalis gen. nov., sp. nov., novel filamentous anaerobes, and description of the new classes Anaerolineae classis nov. and Caldilineae classis nov. in the. International Journal of Systematic and Evolutionary Microbiology, 56, 1331–1340. PubMed

Yurkov, V. and Csotonyi, J.T. (2009) New light on aerobic Anoxygenic phototrophs. In Advances in photosynthesis and respiration. Daldal F, Thurnauer MC, Beatty J. (ed). Springer, Dordrecht, The Netherlands, pp. 31–55.

Yutin, N. , Suzuki, M.T. & Béjà, O. (2005) Novel primers reveal wider diversity among marine aerobic anoxygenic phototrophs. Applied and Environmental Microbiology, 71, 8958–8962. PubMed PMC

Zemskaya, T.I. , Cabello‐Yeves, P.J. , Pavlova, O.N. & Rodriguez‐Valera, F. (2020) Microorganisms of Lake Baikal—the deepest and most ancient lake on earth. Applied Microbiology and Biotechnology, 104, 6079–6090. PubMed

Zeng, Y. , Nupur, W. , N., Madsen, A.M. , Chen, X. , Gardiner, A.T. et al. (2021) Gemmatimonas groenlandica sp. nov. is an aerobic Anoxygenic phototroph in the phylum Gemmatimonadetes. Frontiers in Microbiology, 11, 1–18. PubMed PMC

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