Abstract
A bacteriochlorophyll-containing bacterium, designated as strain N10T, was isolated from a terrestrial hot spring in Nagano Prefecture, Japan. Gram-stain-negative, oxidase- and catalase-positive and ovoid to rod-shaped cells showed the features of aerobic anoxygenic phototrophic bacteria, i.e., strain N10T synthesised bacteriochlorophylls under aerobic conditions and could not grow anaerobically even under illumination. Genome analysis found genes for bacteriochlorophyll and carotenoid biosynthesis, light-harvesting complexes and type-2 photosynthetic reaction centre in the chromosome. Phylogenetic analyses based on the 16S rRNA gene sequence and 92 core proteins revealed that strain N10T was located in a distinct lineage near the type species of the genera Tabrizicola and Xinfangfangia and some species in the genus Rhodobacter (e.g., Rhodobacter blasticus). Strain N10T shared < 97.1% 16S rRNA gene sequence identity with those species in the family Rhodobacteraceae. The digital DNA–DNA hybridisation, average nucleotide identity and average amino acid identity values with the relatives, Tabrizicola aquatica RCRI19T (an aerobic anoxygenic phototrophic bacterium), Xinfangfangia soli ZQBWT and R. blasticus ATCC 33485T were 19.9–20.7%, 78.2–79.1% and 69.1–70.1%, respectively. Based on the phenotypic features, major fatty acid and polar lipid compositions, genome sequence and phylogenetic position, a novel genus and species are proposed for strain N10T, to be named Neotabrizicola shimadae (= JCM 34381T = DSM 112087T). Strain N10T which is phylogenetically located among aerobic anoxygenic phototrophic bacteria (Tabrizicola), bacteriochlorophyll-deficient bacteria (Xinfangfangia) and anaerobic anoxygenic phototrophic bacteria (Rhodobacter) has great potential to promote studies on the evolution of photosynthesis in Rhodobacteraceae.
Similar content being viewed by others
References
Beatty JT (2002) On the natural selection and evolution of the aerobic phototrophic bacteria. Photosynth Res 73:109–114
Boldareva-Nuianzina EN, Bláhová Z, Sobotka R, Koblízek M (2013) Distribution and origin of oxygen-dependent and oxygen-independent forms of Mg-protoporphyrin monomethylester cyclase among phototrophic Proteobacteria. Appl Environ Microbiol 79:2596–2604
Brinkmann H, Göker M, Koblížek M et al (2018) Horizontal operon transfer, plasmids, and the evolution of photosynthesis in Rhodobacteraceae. ISME J 12:1994–2010
Eckersley K, Dow C (1980) Rhodopseudomonas blastica sp. nov.: a member of the Rhodospirillaceae. Microbiology 119:465–473
Everroad CR, Otaki H, Matsuura K, Haruta S (2012) Diversification of bacterial community composition along a temperature gradient at a thermal spring. Microbes Environ 27:374–381
Felsenstein J (1981) Evolutionary trees from DNA sequences: a maximum likelihood approach. J Mol Evol 17:368–376
Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791
Goris J, Konstantinidis KT, Klappenbach JA, Coenye T, Vandamme P, Tiedje JM (2007) DNA–DNA hybridization values and their relationship to whole-genome sequence similarities. Int J Syst Evol Microbiol 57:81–91
Hamada M, Iino T, Iwami T, Harayama S, Tamura T, Suzuki K-I (2010) Mobilicoccus pelagius gen. nov., sp. nov. and Piscicoccus intestinalis gen. nov., sp. nov., two new members of the family Dermatophilaceae, and reclassification of Dermatophilus chelonae (Masters et al. 1995) as Austwickia chelonae gen. nov., comb. nov. J Gen Appl Microbiol 56:427–436
Han JE, Kang W, Lee JY et al (2020) Tabrizicola piscis sp. nov., isolated from the intestinal tract of a Korean indigenous freshwater fish, Acheilognathus koreensis. Int J Syst Evol Microbiol 70:2305–2311
Hanada S, Hiraishi A, Shimada K, Matsuura K (1995) Chloroflexus aggregans sp. nov., a filamentous phototrophic bacterium which forms dense cell aggregates by active gliding movement. Int J Syst Bacteriol 45:676–681
Hirose S, Matsuura K, Haruta S (2016) Phylogenetically diverse aerobic anoxygenic phototrophic bacteria isolated from epilithic biofilms in Tama River, Japan. Microbes Environ 31:299–306
Hördt A, García LM, Meier-Kolthoff JP, Schleuning M, Weinhold L-M, Tindall BJ, Gronow S, Kyrpides NC, Woyke T, Göker M (2020) Analysis of 1,000+ type-strain genomes substantially improves taxonomic classification of Alphaproteobacteria. Front Microbiol 11:468
Hu Q, Zhang L, Hang P, Zhou XY, Jia WB, Li SP, Jiang JD (2018) Xinfangfangia soli gen. nov., sp. nov., isolated from a diuron-polluted soil. Int J Syst Evol Microbiol 68:2622–2626
Imhoff JF (2015) Genus Rhodobacter. In: Whitman WB, Rainey F, Kämpfer P, Trujillo M, Chun J, DeVos P, Hedlund B, Dedysh S (eds) Bergey’s manual of systematics of archaea and bacteria. Wiley, New York
Imhoff JF, Rahn T, Künzel S, Neulinger SC (2018) Photosynthesis is widely distributed among Proteobacteria as demonstrated by the phylogeny of PufLM reaction center proteins. Front Microbiol 23:2679
Imhoff JF, Rahn T, Künzel S, Neulinger SC (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
Jørgensen NOG, Stepanaukas R, Pedersen AGU, Hansen M, Nybroe O (2003) Occurrence and degradation of peptidoglycan in aquatic environments. FEMS Microbiol Ecol 46:269–280
Kämpfer P, Busse HJ, McInroy JA, Criscuolo A, Clermont D, Glaeser SP (2019) Xinfangfangia humi sp. nov., isolated from soil amended with humic acid. Int J Syst Evol Microbiol 69:2070–2075
Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120
Kolber ZS, Plumley FG, Lang AS, Beatty JT, Blankenship RE, VanDover CL, Vetriani C, Koblizek M, Rathgeber C, Falkowski PG (2001) Contribution of aerobic photoheterotrophic bacteria to the carbon cycle in the ocean. Science 292:2492–2495
Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874
Lee I, Kim YO, Park SC, Chun J (2016) OrthoANI: an improved algorithm and software for calculating average nucleotide identity. Int J Syst Evol Microbiol 66:1100–1103
Liu Y, Zheng Q, Lin W, Jiao N (2019) Characteristics and evolutionary analysis of photosynthetic gene clusters on extrachromosomal replicons: from streamlined plasmids to chromids. mSystems 4:e00358-19
Meier-Kolthoff JP, Auch AF, Klenk HP, Göker M (2013) Genome sequence-based species delimitation with confidence intervals and improved distance functions. BMC Bioinform 14:60
Meier-Kolthoff JP, Klenk HP, Göker M (2014) Taxonomic use of DNA G+C content and DNA-DNA hybridization in the genomic age. Int J Syst Evol Microbiol 64:352–356
Minnikin DE, Collins MD, Goodfellow M (1979) Fatty acid and polar lipid composition in the classification of Cellulomonas, Oerskovia and related taxa. J Appl Bacteriol 47:87–95
Molisch H (1907) Die Purpurbakterien: nach neueren untersuchungen. Gustav Fischer Verlag, Jena, pp 1–95
Na SI, Kim YO, Yoon SH, Ha SM, Baek I, Chun J (2018) UBCG: up-to-date bacterial core gene set and pipeline for phylogenomic tree reconstruction. J Microbiol 56:280–285
Reasoner DJ, Geldreich EE (1985) A new medium for the enumeration and subculture of bacteria from potable water. Appl Environ Microbiol 49:1–7
Rodriguez-R LM, Konstantinidis KT (2014) Bypassing cultivation to identify bacterial species. Microbe 9:111–118
Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425
Sasser M (2001) Identification of bacteria by gas chromatography of cellular fatty acids, MIDI technical note 101. MIDI Inc, Newark
Seemann T (2014) Prokka: rapid prokaryotic genome annotation. Bioinformatics 30:2068–2069
Sheu C, Li ZH, Sheu SY, Yang CC, Chen WM (2020) Tabrizicola oligotrophica sp. nov. and Rhodobacter tardus sp. nov., two new species of bacteria belonging to the family Rhodobacteraceae. Int J Syst Evol Microbiol 70:6266–6283
Shimada K (1995) Aerobic anoxygenic phototrophs. In: Blankenship RE, Madigan MT, Bauer CE (eds) Anoxygenic photosynthetic bacteria. Advances in photosynthesis and respiration, vol 2. Springer, Dordrecht, pp 105–122
Suresh G, Lodha TD, Indu B, Sasikala C, Ramana CV (2019) Taxogenomics resolves conflict in the genus Rhodobacter: a two and half decades pending thought to reclassify the genus Rhodobacter. Front Microbiol 10:2480
Tanizawa Y, Fujisawa T, Nakamura Y (2018) DFAST: a flexible prokaryotic genome annotation pipeline for faster genome publication. Bioinformatics 34:1037–1039
Tarhriz V, Thiel V, Nematzadeh G, Hejazi MA, Imhoff JF, Hejazi MS (2013) Tabrizicola aquatica gen. nov. sp. nov., a novel alphaproteobacterium isolated from Qurugöl Lake nearby Tabriz city, Iran. Antonie Van Leeuwenhoek 104:1205–1215
Tarhriz V, Hirose S, Fukushima SI, Hejazi MA, Imhoff JF, Thiel V, Hejazi MS (2019) Emended description of the genus Tabrizicola and the species Tabrizicola aquatica as aerobic anoxygenic phototrophic bacteria. Antonie Van Leeuwenhoek 112:1169–1175
Thiel V, Tank M, Bryant DA (2018) Diversity of chlorophototrophic bacteria revealed in the omics era. Annu Rev Plant Biol 69:21–49
Wick RR, Judd LM, Gorrie CL, Holt KE (2017) Unicycler: Resolving bacterial genome assemblies from short and long sequencing reads. PLoS Comput Biol 13:1–22
Yurkov V, Csotonyi JT (2009) New light on aerobic anoxygenic phototrophs. In: Hunter CN, Daldal F, Thurnauer MC, Beatty JT (eds) The purple phototrophic bacteria. Advances in photosynthesis and respiration, vol 28. Springer, Dordrecht, pp 31–55
Yurkov V, Hughes E (2017) Aerobic anoxygenic phototrophs: four decades of mystery. In: Hallenbeck PC (ed) Modern topics in the phototrophic prokaryotes. Springer, Cham, pp 193–214
Zeng Y, Feng F, Medová H, Dean J, Koblížek M (2014) Functional type 2 photosynthetic reaction centers found in the rare bacterial phylum Gemmatimonadetes. Proc Natl Acad Sci USA 111:7795–7800
Zheng Q, Zhang R, Koblížek M, Boldareva EN, Yurkov V et al (2011) Diverse arrangement of photosynthetic gene clusters in aerobic anoxygenic phototrophic bacteria. PLoS ONE 6:e25050
Zsebo KM, Hearst JE (1984) Genetic-physical mapping of a photosynthetic gene cluster from R. capsulata. Cell 37:937–947
Acknowledgements
We thank Mr. Takahito Momose (the owner of Nakabusa hot springs) for allowing us to collect samples from the hot springs. We also thank Prof. Aharon Oren (The Hebrew University of Jerusalem) for helpful corrections of the proposed name and its etymology.
Funding
This research was supported by a research grant from the Institute for Fermentation, Osaka.
Author information
Authors and Affiliations
Contributions
SM, SHn and SHr planned the research. SM and SHi carried out experiments. SM, TI and SHr analysed the data and drafted the manuscript. MO and SHn supervised the research and SHn provided the research funding. All authors proofread the manuscript.
Corresponding author
Ethics declarations
Conflict of interests
The authors declare that there are no conflicts of interest.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Muramatsu, S., Hirose, S., Iino, T. et al. Neotabrizicola shimadae gen. nov., sp. nov., an aerobic anoxygenic phototrophic bacterium harbouring photosynthetic genes in the family Rhodobacteraceae, isolated from a terrestrial hot spring. Antonie van Leeuwenhoek 115, 731–740 (2022). https://doi.org/10.1007/s10482-022-01728-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10482-022-01728-6