Diverse aerobic anoxygenic phototrophs synthesize bacteriochlorophyll in oligotrophic rather than copiotrophic conditions, suggesting ecological niche.


Journal

Environmental microbiology
ISSN: 1462-2920
Titre abrégé: Environ Microbiol
Pays: England
ID NLM: 100883692

Informations de publication

Date de publication:
11 2023
Historique:
received: 07 02 2023
accepted: 01 08 2023
medline: 15 11 2023
pubmed: 22 8 2023
entrez: 21 8 2023
Statut: ppublish

Résumé

While investigating aerobic anoxygenic phototrophs (AAP) from Lake Winnipeg's bacterial community, over 500 isolates were obtained. Relatives of 20 different species were examined simultaneously, identifying conditions for optimal growth or pigment production to determine features that may unify this group of phototrophs. All were distributed among assorted α-Proteobacterial families including Erythrobacteraceae, Sphingomonadaceae, Sphingosinicellaceae, Acetobacteraceae, Methylobacteriaceae, and Rhodobacteraceae. Major phenotypic characteristics matched phylogenetic association, including pigmentation, morphology, metal transformations, tolerances, lipid configurations, and enzyme activities, which distinctly separated each taxonomic family. While varying pH and temperature had a limited independent impact on pigment production, bacteriochlorophyll synthesis was distinctly promoted under low nutrient conditions, whereas copiotrophy repressed its production but enhanced carotenoid yield. New AAP diversity was also reported by revealing strains related to non-phototrophic Rubellimicrobium and Sphingorhabdus, as well as spread throughout Roseomonas, Sphingomonas, and Methylobacterium/Methylorubrum, which previously only had a few known photosynthetic members. This study exemplified the overwhelming diversity of AAP in a single aquatic environment, confirming cultivation continues to be of importance in microbial ecology to discover functionality in both new and previously reported cohorts of bacteria as specific laboratory conditions were required to promote aerobic bacteriochlorophyll production.

Identifiants

pubmed: 37604501
doi: 10.1111/1462-2920.16482
doi:

Substances chimiques

Bacteriochlorophylls 0

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

2653-2665

Informations de copyright

© 2023 The Authors. Environmental Microbiology published by Applied Microbiology International and John Wiley & Sons Ltd.

Références

Aldred, P., Hill, A.C. & Young, C. (1974) The isolation of Streptobacillus moniliformis from cervical abscesses of Guinea-pigs. Laboratory Animals, 8(3), 275-277. Available from: https://doi.org/10.1258/002367774780943670
Bligh, E.G. & Dyer, W.J. (1959) A rapid method of total lipid extraction and purification. Canadian Journal of Biochemistry and Physiology, 37, 911-917.
Bryantseva, I.A., Kyndt, J.A., Gorlenko, V.M. & Imhoff, J.F. (2023) Ectothiorhodospira lacustris sp. nov., a new purple sulfur bacterium from low-mineralized Soda Lakes that contains a unique pathway for nitric oxide reduction. Microorganisms, 11, 1336.
Coordinators, N.R. (2013) Database resources of the national center for biotechnology information. Nucleic Acids Research, 41, 8-20. Available from: https://doi.org/10.1093/nar/gks1189
Csotonyi, J.T., Maltman, C. & Yurkov, V. (2014) Influence of tellurite on synthesis of bacteriochlorophyll and carotenoids in aerobic anoxygenic phototrophic bacteria. Research Trends in Photochemistry & Photobiology, 16, 1-17.
Csotonyi, J.T., Stackebrandt, E., Swiderski, J., Schumann, P. & Yurkov, V. (2011) An alphaproteobacterium capable of both aerobic and anaerobic anoxygenic photosynthesis but incapable of photoautotrophy: Charonomicrobium ambiphototrophicum, gen. nov., sp. nov. Photosynthesis Research, 107, 257-268.
Čuperová, Z., Holzer, E., Salka, I., Sommaruga, R. & Koblížek, M. (2013) Temporal changes and altitudinal distribution of aerobic anoxygenic phototrophs in mountain lakes. Applied and Environmental Microbiology, 79(20), 6439-6446.
Fecskeová, L.K., 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.
Hauruseu, D. & Koblížek, M. (2012) Influence of light on carbon utilization in aerobic anoxygenic phototrophs. Applied and Environmental Microbiology, 78(20), 7414-7419.
Hördt, A., López, M.G., Meier-Kolthoff, J.P., Schleuning, M., Weinhold, L.-M., Tindall, B.J. et al. (2020) Analysis of 1,000+ type-strain genomes substantially improves taxonomic classification of alphaproteobacteria. Frontiers in Microbiology, 11, 468.
Imanishi, M., Takenouchi, M., Takaichi, S., Nakagawa, S., Saga, Y., Takenaka, S. et al. (2019) A dual role for Ca2+ in expanding the spectral diversity and stability of LH1-RC photocomplexes of purple phototrophic bacteria. Biochemistry, 58, 2844-2852.
Kevbrin, V., Boltyanskaya, Y., Koziaeva, V., Uzun, M. & Grouzdev, D. (2021) Alkalicaulis satelles gen. nov., sp. nov., a novel haloalkaliphile isolated from a laboratory culture cyanobacterium Geitlerinema species and proposals of Maricaulaceae fam. nov., Robiginitomaculaceae fam. nov., Maricaulales ord. nov. and Hyphomonadales ord. nov. International Journal of Systematic and Evolutionary Microbiology, 71, 1-14.
Koblížek, M. (2015) Ecology of aerobic anoxygenic phototrophs in aquatic environments. FEMS Microbiology Reviews, 39, 854-870.
Kopejtka, K., Tomasch, J., Zeng, Y., Selyanin, V., Dachev, M., Piwosz, K. et al. (2020) Simultaneous presence of bacteriochlorophyll and xanthorhodopsin genes in a freshwater bacterium. mSystems, 5, e01044-20.
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.
Kumar, S., Stecher, G., Li, M., Knyaz, C. & Tamura, K. (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Molecular Biology and Evolution, 35, 1547-1549.
Kuznetsov, S.I., Dubinina, G.A. & Lapteva, N.A. (1979) Biology of oligotrophic bacteria. Annual Review of Microbiology, 33(1), 377-387.
Kuzyk, S.B., Hughes, E. & Yurkov, V. (2021) Discovery of siderophore and metallophore production in the aerobic anoxygenic phototrophs. Microorganisms, 9(5), 959.
Kuzyk, S.B., Jafri, M., Humphrey, E., Maltman, C., Kyndt, J.A. & Yurkov, V. (2022) Prosthecate aerobic anoxygenic phototrophs Photocaulis sulfatitolerans gen. nov., sp. nov. and Photocaulis rubescens sp. nov. isolated from alpine meromictic lakes in British Columbia, Canada. Archives of Microbiology, 204, 444.
Kuzyk, S.B., Ma, X. & Yurkov, V. (2022) Seasonal dynamics of Lake Winnipeg's microbial communities reveal aerobic anoxygenic phototrophic populations coincide with sunlight availability. Microorganisms, 10(9), 1690.
Kuzyk, S.B., Weins, K., Ma, X. & Yurkov, V. (2020) Association of aerobic anoxygenic phototrophs and zebra mussels, Dreissena polymorpha, within the littoral zone of Lake Winnipeg's south basin. Journal of Great Lakes Research, 47(3), 567-582.
Maltman, C. & Yurkov, V. (2015) The effect of tellurite on highly resistant freshwater aerobic anoxygenic phototrophs and their strategies for reduction. Microorganisms, 3, 826-838.
Manitoba Agriculture and Resource Department (MARD). (2020) State of Lake Winnipeg, 2nd edition. Winnipeg, Manitoba, Canada: Environment and Climate Change Canada, pp. 1-195.
Mašín, M., Nedoma, J., Pechar, L. & Koblížek, M. (2008) Distribution of aerobic anoxygenic phototrophs in temperate freshwater systems. Environmental Microbiology, 10, 1988-1996.
Nei, M. & Kumar, S. (2000) Molecular evolution and phylogenetics. New York, USA: Oxford University Press.
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.
Price, P.B. & Sowers, T. (2004) Temperature dependence of metabolic rates for microbial growth, maintenance, and survival. PNAS, 101(13), 4631-4636.
Pujalte, M.J., Lucena, T., Ruvira, M.A., Arahal, D.R. & Macián, M.C. (2014) The family Rhodobacteraceae. In: Rosenberg, E., DeLong, E.F., Lory, S., Stackebrandt, E. & Thompson, F. (Eds.) The prokaryotes. Berlin, Heidelberg: Springer, pp. 439-512.
Rai, A., Jagadeeshwari, U., Deepshikha, G., Smita, N., Sasikala, C. & Ramana, C.V. (2021) Phylotaxogenomics for the reappraisal of the genus Roseomonas with the creation of six new genera. Frontiers in Microbiology, 12, 677842.
Rathgeber, C., Yurkova, N., Stackebrandt, E., Schumann, P., Beatty, T.J. & Yurkov, V. (2005) Roseicyclus mahoneyensis gen. nov., sp. nov., an aerobic phototrophic bacterium isolated from a meromictic lake. International Journal of Systematic and Evolutionary Microbiology, 55, 1597-1603.
Shimada, K. (1995) Aerobic anoxygenic phototrophs. In: Blankenship, R.E., Madigan, M.T. & Bauer, C.E. (Eds.) Anoxygenic photosynthetic bacteria. Dordrecht: Kluwer Academic Publishers, pp. 105-122.
Suyama, T., Kanno, N., Matsukura, S., Chihara, K., Noda, N. & Hanada, S. (2023) Transcriptome and deletion mutant analyses revealed that an RpoH family sigma factor is essential for photosystem production in Roseateles depolymerans under carbon starvation. Microbes and Environments, 38(1), ME22072.
Tamura, K. & Nei, M. (1993) Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Molecular Biology and Evolution, 10, 512-526.
Wakao, N., Yokoi, N., Isoyama, N., Hiraishi, A., Shimada, K., Kobayashi, M. et al. (1996) Discovery of natural photosynthesis using Zn-containing bacteriochlorophyll in an aerobic bacterium Acidiphilium rubrum. Plant & Cell Physiology, 37(6), 889-893.
Yurkov, V. & Beatty, J.T. (1998) Aerobic anoxygenic phototrophic bacteria. Microbiology and Molecular Biology Reviews, 62, 695-724.
Yurkov, V., Gadon, N. & Drews, G. (1993) The major part of polar carotenoids of the aerobic bacteria Roseococcus thiosulfatophilus, RB3 and Erythromicrobium ramosum, E5 is not bound to the bacteriochlorophyll a-complexes of the photosynthetic apparatus. Archives of Microbiology, 160, 372-376.
Yurkov, V. & Gorlenko, V.M. (1992) A new genus of freshwater aerobic bacteriochlorophyll-a containing bacteria Roseococcus gen. nov. Microbiology (New York), 60, 628-630.
Yurkov, V. & Hughes, E. (2013) Genes associated with the peculiar phenotypes of the aerobic anoxygenic phototrophs. In: Blankenship, R.E. (Ed.) Advances in Botanical Research. The genome evolution of photosynthetic bacteria, Vol. 66. Amsterdam, The Netherlands: Elsevier, pp. 327-358.
Yurkov, V. & Hughes, E. (2017) Aerobic anoxygenic phototrophs: four decades of mystery. In: Patrick, C. (Ed.) Modern topics in the phototrophic prokaryotes: metabolism, bioenergetics and omics. Hallenbeck: Springer, pp. 193-217.
Yurkov, V., Jappe, J. & Vermeglio, A. (1996) Tellurite resistance and reduction by obligatory aerobic photosynthetic bacteria. Applied and Environmental Microbiology, 11, 4195-4198.
Yurkov, V., Stackebrandt, E., Holmes, A., Fuerst, J.A., Hugenholtz, P., Golecki, J. et al. (1994) Phylogenetic positions of novel aerobic, bacteriochlorophyll a-containing bacteria and description of Roseococcus thiosulfatophilus gen. nov., sp. nov., Erythromicrobium ramosum gen. nov., sp. nov., and Erythrobacter litoralis sp. nov. International Journal of Systematic Bacteriology, 44, 427-434.
Yurkov, V. & van Gemerden, H. (1993) Impact of light/dark regime on growth rate, biomass formation and bacteriochlorophyll synthesis in Erythromicrobium hydrolyticum. Archives of Microbiology, 159, 84-89.
Zeng, Y., Nupur, W.N., Madsen, A.M., Chen, X., Gardiner, A.T. & Koblížek, M. (2021) Gemmatimonas groenlandica sp. nov. is an aerobic anoxygenic phototroph in the phylum Gemmatimonadetes. Frontiers in Microbiology, 11, 606612.
Zervas, A., Zeng, Y., Madsen, A.M. & Hansen, L.H. (2019) Genomics of aerobic photoheterotrophs in wheat phyllosphere reveals divergent evolutionary patterns of photosynthetic genes in Methylobacterium spp. Genome Biology and Evolution, 11, 2895-2908.

Auteurs

Steven B Kuzyk (SB)

Department of Microbiology, University of Manitoba, Winnipeg, Manitoba, Canada.

Katia Messner (K)

Department of Microbiology, University of Manitoba, Winnipeg, Manitoba, Canada.

Jocelyn Plouffe (J)

Department of Microbiology, University of Manitoba, Winnipeg, Manitoba, Canada.

Xiao Ma (X)

Department of Microbiology, University of Manitoba, Winnipeg, Manitoba, Canada.

Kaitlyn Wiens (K)

Department of Microbiology, University of Manitoba, Winnipeg, Manitoba, Canada.

Vladimir Yurkov (V)

Department of Microbiology, University of Manitoba, Winnipeg, Manitoba, Canada.

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