Abstract
This article reports the results of quantitative intra- and intergeneric taxonomic relationships among Micrococcaceae strains and a novel endophytic bacterium (SG) isolated from a suspension culture of Arabidopsis thaliana (L.) Heynh in our laboratory. The known strain Rothia sp. ND6WE1A was used as a reference one for SG. Whole-genome sequencing and phylogenetic analysis were based on the 16S rRNA test. Quantitative analysis for the nucleotide identity (ANI) and calculation of evolutionary distances were based on the identified amino acids (AAI) test indicating the generic assignment of the reference strain within and between the identified monophyletic groups of Micrococcaceae. The amino acid data structure of Rothia sp. ND6WE1A was compared against the UniProt database (250 million records) of close lineage of Micrococcaceae, including other Rothia spp. These data presented unique and evolutionary amino acid alignments, eventually expected in the new SG isolate as well. The metagenomic entries of the respective genome and proteome, characterized at the genus and species levels, could be considered for evolutionary taxonomic reclassification of the isolated and the reference strain (SG + Rothia sp. ND6WE1A). Therefore, our results warrant further investigations on the isolated SG strain.
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The datasets generated during and/or analysed during the current study are available from the corresponding author on reasonable request.
References
AAI-profiler: fast proteome-wide search reveals taxonomic outliers. http://ekhidna2.biocenter.helsinki.fi/AAI. Accessed 18 Sept 2023
ANI/AAI-Matrix. Genome-based distance matrix calculator. http://enve-omics.ce.gatech.edu/g-matrix. Accessed 18 Sept 2023
Archaeopteryx. https://sites.google.com/site/cmzmasek/christian-zmasek/software/archaeopteryx?authuser=0. Accessed 18 Sept 2023.
Asadu CO, Ike IS, Onu CE, Egbuna SO, Onoh M, Mbah GO, Eze CN (2020) Investigation of the influence of biofertilizer synthesized using microbial inoculums on the growth performance of two agricultural crops. Biotechnol Rep 27:e00493. https://doi.org/10.1016/j.btre.2020.e00493
Asyakina LK, Vorob’eva EE, Proskuryakova LA, Zharko MY (2023) Evaluating extremophilic microorganisms in industrial regions. Foods Raw Mater 11:162–171. https://doi.org/10.21603/2308-4057-2023-1-556
Austin B (2015) Rothia. In: Whitman WB (ed) Bergey’s manual of systematics of archaea and bacteria. Wiley, Hoboken, pp 1–13. https://doi.org/10.1002/9781118960608.gbm00124
Bano A, Muqarab R (2017) Plant defense induced by PGPR against Spodoptera litura in tomato (Solanum lycopersicum L.). Plant Biol 19:406–412. https://doi.org/10.1111/plb.12535
Borah A, Thakur D (2020) Phylogenetic and functional characterization of culturable endophytic actinobacteria associated with Camellia spp. for growth promotion in commercial tea cultivars. Front Microbiol 11:318. https://doi.org/10.3389/fmicb.2020.00318
Chaumeil P-A, Mussig AJ, Hugenholtz P, Parks DH (2022) GTDB-Tk v2: memory friendly classification with the genome taxonomy database. Bioinformatics 38:5315–5316. https://doi.org/10.1093/bioinformatics/btac672
Collection of Rhizosphere Microorganisms. https://collection.ibppm.ru. Accessed 18 Sept 2023
da Silva JCP, de Medeiros FHV, Campos VP (2018) Building soil suppressiveness against plant-parasitic nematodes. Biocontrol Sci Technol 28:423–445. https://doi.org/10.1080/09583157.2018.1460316
Davis I, Sevigny J, Kleiner V, Mercurio K, Pesce C, Swanson E, Thomas WK, Tisa LS (2020) Draft genome sequences of 10 bacterial strains isolated from root nodules of Alnus trees in New Hampshire. Microbiol Resour Announc 9:e01440-e1519. https://doi.org/10.1128/MRA.01440-19
de Oliveira IMF, Ng DYK, van Baarlen P, Stegger M, Andersen PS, Wells JM (2022) Comparative genomics of Rothia species reveals diversity in novel biosynthetic gene clusters and ecological adaptation to different eukaryotic hosts and host niches. Microb Genom 8:mgmen000854. https://doi.org/10.1099/mgen.0.000854
Elbahnasawy MA, Shehabeldine AM, Khattab AM, Amin BH, Hashem AH (2021) Green biosynthesis of silver nanoparticles using novel endophytic Rothia endophytica: characterization and anticandidal activity. J Drug Deliv Sci Technol 62:102401. https://doi.org/10.1016/j.jddst.2021.102401
Evangelista EV, Garcia FC, Cruz JA (2017) Isolation, characterization and identification of plant growth-promoting rhizobacteria. Int J Agric Technol 13:715–727
Fan Y, Jin Z, Tong J, Li W, Pasciak M, Gamian A, Liu Z, Huang Y (2002) Rothia amarae sp. nov., from sludge of a foul water sewer. Int J Syst Evol Microbiol 52:2257–2260. https://doi.org/10.1099/00207713-52-6-2257
FastME 2.0: a comprehensive, accurate, and fast distance-based phylogeny inference program. http://www.atgc-montpellier.fr/fastme. Accessed 18 Sept 2023.
Fatahi-Bafghi M (2021) Characterization of the Rothia spp. and their role in human clinical infections. Infect Genet Evol 93:104877. https://doi.org/10.1016/j.meegid.2021.104877
Genome Information by Organism. https://www.ncbi.nlm.nih.gov/genome/browse/#!/overview. Accessed 18 Sept 2023
Genome taxonomy database. https://gtdb.ecogenomic.org. Accessed 18 Sept 2023.
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. https://doi.org/10.1099/ijs.0.64483-0
Gtari M, Ghodhbane-Gtari F, Nouioui I, Beauchemin N, Tisa LS (2012) Phylogenetic perspectives of nitrogen-fixing actinobacteria. Arch Microbiol 194:3–11. https://doi.org/10.1007/s00203-011-0733-6
GTDB Data. Index of /releases/release202/202.0/. https://data.gtdb.ecogenomic.org/releases/release202/202.0/. Accessed 18 Sept 2023
GTDB-Tk Classify-v1.6.0. https://kbase.us/applist/apps/kb_gtdbtk/run_kb_gtdbtk. Accessed 18 Sept 2023.
Guénoche A, Garreta H (2000) Can we have confidence in a tree representation? In: Gascuel O, Sagot MF (eds) Computational biology. JOBIM 2000. Lecture Notes in Computer Science, vol 2066. Springer. Berlin, Heidelberg, pp 45–56. https://doi.org/10.1007/3-540-45727-5_5
Jain C, Rodriguez-R LM, Phillippy AM, Konstantinidis KT, Aluru S (2018) High throughput ANI analysis of 90K prokaryotic genomes reveals clear species boundaries. Nat Commun 9:5114. https://doi.org/10.1038/s41467-018-07641-9
Jia Y, Li X, Xu F, Liu Z, Fu Y, Xu X, Yang J, Zhang S, Shen C (2022) Single-cell-level microfluidics assisted with resuscitation-promoting factor technology (SMART) to isolate novel biphenyl-degrading bacteria from typical soils in eastern China. Environ Pollut 311:119864. https://doi.org/10.1016/j.envpol.2022.119864
Kim M, Oh HS, Park SC, Chun J (2014) Towards a taxonomic coherence between average nucleotide identity and 16S rRNA gene sequence similarity for species demarcation of prokaryotes. Int J Syst Evol Microbiol 64:346–351. https://doi.org/10.1099/ijs.0.059774-0
Ko KS, Lee MY, Park YK, Peck KR, Song J-H (2009) Molecular identification of clinical Rothia isolates from human patients: proposal of a novel Rothia species, Rothia arfidiae sp. nov. J Bacteriol Virol 39:159–164. https://doi.org/10.4167/jbv.2009.39.3.159
Konstantinidis KT, Tiedje JM (2007) Prokaryotic taxonomy and phylogeny in the genomic era: advancements and challenges ahead. Curr Opin Microbiol 10:504–509. https://doi.org/10.1016/j.mib.2007.08.006
Koonin EV (2012) The logic of chance: the nature and origin of biological evolution. Pearson Education, Upper Saddle River
Lefort V, Desper R, Gascuel O (2015) FastME 2.0: a comprehensive, accurate, and fast distance-based phylogeny inference program. Mol Biol Evol 32:2798–2800. https://doi.org/10.1093/molbev/msv150
Lemoine F, Entfellner J-BD, Wilkinson E, Correia D, Felipe MD, De Oliveira T, Gascuel O (2018) Renewing Felsenstein’s phylogenetic bootstrap in the era of big data. Nature 556:452–456. https://doi.org/10.1038/s41586-018-0043-0
Lemoine F, Correia D, Lefort V, Doppelt-Azeroual O, Mareuil F, Cohen-Boulakia S, Gascuel O (2019) NGPhylogeny.fr: new generation phylogenetic services for non-specialists. Nucleic Acids Res 47:W260–W265. https://doi.org/10.1093/nar/gkz303
Luo C, Rodriguez-R LM, Konstantinidis KT (2014) MyTaxa: an advanced taxonomic classifier for genomic and metagenomic sequences. Nucleic Acids Res 42:e73. https://doi.org/10.1093/nar/gku169
Mažeikienė I, Frercks B, Burokienė D, Mačionienė I, Šalaševičiene A (2021) Endophytic community composition and genetic-enzymatic features of cultivable bacteria in Vaccinium myrtillus L. in forests of the Baltic-Nordic region. Forests 12:1647. https://doi.org/10.3390/f12121647
Medlar AJ, Törönen P, Holm L (2018) AAI-profiler: fast proteome-wide exploratory analysis reveals taxonomic identity, misclassification and contamination. Nucleic Acids Res 46:W479–W485. https://doi.org/10.1093/nar/gky359
MEGA. Molecular Evolutionary Genetics Analysis. https://www.megasoftware.net. Accessed 18 September 2023.
Mercurio K, Sevigny J, Pesce C, Thomas WK, Tisa LS (2022) Draft genome sequences for bacteria associated with root nodules of Alnus incana in New England. Microbiol Resour Announc 11:e0091422. https://doi.org/10.1128/mra.00914-22
Nardone G, Compare D (2015) The human gastric microbiota: is it time to rethink the pathogenesis of stomach diseases? United Eur Gastroenterol J 3:255–260. https://doi.org/10.1177/2050640614566846
New query datasets. https://disc-genomics.uibk.ac.at/miga/query_datasets/new?project_id=4. Accessed 18 Sept 2023
NGPhylogeny.fr. https://ngphylogeny.fr. Accessed 18 Sept 2023
Nuaima RH (2022) The difference in the bacterial attachment among Pratylenchus neglectus populations and its effect on the nematode infection. Microorganisms 10:1524. https://doi.org/10.3390/microorganisms10081524
Odeberg G, Bläckberg A, Sunnerhagen T (2023) Infection or contamination with Rothia, Kocuria, Arthrobacter and Pseudoglutamicibacter—a retrospective observational study of non-Micrococcus Micrococcaceae in the clinic. J Clin Microbiol 61:e0148422. https://doi.org/10.1128/jcm.01484-22
Opelt K, Berg C, Berg G (2007) The bryophyte genus Sphagnum is a reservoir for powerful and extraordinary antagonists and potentially facultative human pathogens. FEMS Microbiol Ecol 61:38–53. https://doi.org/10.1111/j.1574-6941.2007.00323.x
Oren A, Garrity GM (2014) Then and now: a systematic review of the systematics of prokaryotes in the last 80 years. Antonie Van Leeuwenhoek 106:43–56. https://doi.org/10.1007/s10482-013-0084-1
Parks DH, Rinke C, Chuvochina M, Chaumeil P-A, Woodcroft BJ, Evans PN, Hugenholtz P, Tyson GW (2017) Recovery of nearly 8,000 metagenome-assembled genomes substantially expands the tree of life. Nat Microbiol 2:1533–1542. https://doi.org/10.1038/s41564-017-0012-7
Parks DH, Chuvochina M, Waite DW, Rinke C, Skarshewski A, Chaumeil P-A, Hugenholtz P (2018) A standardized bacterial taxonomy based on genome phylogeny substantially revises the tree of life. Nat Biotechnol 36:996–1004. https://doi.org/10.1038/nbt.4229
Parks DH, Chuvochina M, Chaumeil P-A, Rinke C, Mussig AJ, Hugenholtz P (2020) A complete domain-to-species taxonomy for Bacteria and Archaea. Nat Biotechnol 38:1079–1086. https://doi.org/10.1038/s41587-020-0501-8
Petrović M, Janakiev T, Grbić ML, Unković N, Stević T, Vukićević S, Dimkić S (2024) Insights into endophytic and rhizospheric bacteria of five sugar beet hybrids in terms of their diversity, plant-growth promoting, and biocontrol properties. Microb Ecol 87:19. https://doi.org/10.1007/s00248-023-02329-0
Pisarska K, Pietr SJ (2015) Biodiversity of dominant cultivable endophytic bacteria inhabiting tissues of six different cultivars of maize (Zea mays L. ssp. mays) cropped under field conditions. Pol J Microbiol 64:163–170. https://doi.org/10.33073/pjm-2015-024
REQ. https://gitlab.pasteur.fr/GIPhy/REQ. Accessed 18 Sept 2023
Rodriguez-R LM, Konstantinidis KT (2014) Bypassing cultivation to identify bacterial species. Microbe 9:111–118. https://doi.org/10.1128/MICROBE.9.111.1
Rodriguez-R LM, Gunturu S, Harvey WT, Rossello-Mora R, Tiedje JM, Cole JR, Konstantinidis KT (2018) The Microbial Genomes Atlas (MiGA) webserver: taxonomic and gene diversity analysis of Archaea and Bacteria at the whole genome level. Nucleic Acids Res 46:W282–W288. https://doi.org/10.1093/nar/gky467
Rodriguez-R LM, Harvey WT, Rosselló-Mora R, Tiedje JM, Cole JR, Konstantinidis KT (2020) Classifying prokaryotic genomes using the Microbial Genomes Atlas (MiGA) webserver. In: Whitman WB (ed) Bergey’s manual of systematics of archaea and bacteria. Wiley, Hoboken, pp 1–11. https://doi.org/10.1002/9781118960608.bm00042
Search EzBioCloud Database. https://www.ezbiocloud.net. Accessed 18 Sept 2023
Sekhar AC, Thomas P (2015) Isolation and identification of shoot-tip associated endophytic bacteria from banana cv. Grand Naine and testing for antagonistic activity against Fusarium oxysporum f. sp. cubense. Am J Plant Sci 6:943–954. https://doi.org/10.4236/ajps.2015.67101
Shchyogolev SY, Dykman LA, Sokolov AO, Sokolov OI (2023) Matora LY (2023) Elimination of contamination in the published 16S rRNA gene sequence of Rothia amarae type strain J18T during phylogenetic studies of a bacterial isolate from a suspension cell culture of Arabidopsis thaliana (Heynh.). BioRxiv 6:273. https://doi.org/10.1101/2023.11.08.566172
Shurigin V, Egamberdieva D, Li L, Davranov K, Panosyan H, Birkeland N-K, Wirth S, Bellingrath-Kimura SD (2020) Endophytic bacteria associated with halophyte Seidlitzia rosmarinus Ehrenb. ex Boiss. from saline soil of Uzbekistan and their plant beneficial traits. J Arid Land 12:730–740. https://doi.org/10.1007/s40333-020-0019-4
Sokolov AO, Dykman LA, Galitskaya AA, Sokolov OI (2021) Identification and characterization of Rothia amarae sp. nov. in a suspension culture of Arabidopsis thaliana (Heynh.) cells. Biol Life Sci Forum 4:92. https://doi.org/10.3390/IECPS2020-08753
Sokolova EA, Mishukova OV, Hlistun IV, Tromenschleger IN, Tikunov AY, Manakhov AD, Rogaev EI, Savenkov OA, Buyanova MD, Ivanov IV, Smirnova NV, Voronina EN (2024) The effectiveness of co-inoculation by consortia of microorganisms depends on the type of plant and the soil microbiome. Plants 13:116. https://doi.org/10.3390/plants13010116
Stackebrandt E, Ebers J (2006) Taxonomic parameters revisited: tarnished gold standards. Microbiol Today 33:152–155
Stubbendieck RM, Dissanayake E, Burnham PM, Zelasko SE, Temkin MI, Wisdorf SS, Vrtis RF, Gern JE, Currie CR (2023) Rothia from the human nose inhibit Moraxella catarrhalis colonization with a secreted peptidoglycan endopeptidase. mBio 14:e0046423. https://doi.org/10.1128/mbio.00464-23
SYNTOL. http://www.syntol.ru. Accessed 18 Sept 2023
Tettelin H, Medini D (eds) (2020) The Pangenome. In: Diversity, dynamics and evolution of genomes. Springer, Cham
Tindall BJ, Rosselló-Móra R, Busse HJ, Ludwig W, Kämpfer P (2010) Notes on the characterization of prokaryote strains for taxonomic purposes. Int J Syst Evol Microbiol 60:249–266. https://doi.org/10.1099/ijs.0.016949-0
Torche A, Benhizia H, Rosselli R, Romoli O, Zanardo M, Baldan E, Alberghini S, Tondello A, Baldan B, Benguedouar A, Squartini A, Benhizia Y (2014) Characterization of bacteria associated with nodules of two endemic legumes of Algeria, Hedysarum naudinianum and H. perrauderianum. Ann Microbiol 64:1065–1071. https://doi.org/10.1007/s13213-013-0745-3
Treangen TJ, Rocha EPC (2011) Horizontal transfer, not duplication, drives the expansion of protein families in prokaryotes. PLoS Genet 7:e1001284. https://doi.org/10.1371/journal.pgen.1001284
Tuikhar N, Kirdat K, Nair G, Padma S, Thorat V, Swetha P, Sathe S, Sundararaj R, Yadav A (2022) Rothia santali sp. nov. endophytic bacteria isolated from sandalwood (Santalum album L.) seedling. Arch Microbiol 204:609. https://doi.org/10.1007/s00203-022-03237-6
Understanding Results. https://help.microbial-genomes.org/understanding-results#distance. Accessed 18 Sept 2023
UniProtKB. Find your protein. https://www.uniprot.org. Accessed 18 Sept 2023
Vaghari Souran SE, Shekariesfahlan A, Ashrafi F, Naeimi S, Ghasemi A (2023) Isolation and identification of grapevine endophytic bacteria with antagonistic potential against Fomitiporia mediterranea, a pathogen involved in grapevine trunk disease. J Plant Dis Prot 130:1371–1384. https://doi.org/10.1007/s41348-023-00788-8
Xiao Y, Chen L, Teng K, Ma J, Xiang S, Jiang L, Liu G, Yang B, Fang J (2023) Potential roles of the rhizospheric bacterial community in assisting Miscanthus floridulus in remediating multi-metal(loid)s contaminated soils. Environ Res 227:115749. https://doi.org/10.1016/j.envres.2023.115749
Xiong Z-J, Zhang J-L, Zhang D-F, Zhou Z-L, Liu M-J, Zhu W-Y, Zhao L-X, Xu L-H, Li W-J (2013) Rothia endophytica sp. nov., an actinobacterium isolated from Dysophylla stellata (Lour.) Benth. Int J Syst Evol Microbiol 63:3964–3969. https://doi.org/10.1099/ijs.0.052522-0
Yarza P, Yilmaz P, Pruesse E, Glöckner FO, Ludwig W, Schleifer KH, Whitman WB, Euzéby J, Amann R, Rosselló-Móra R (2014) Uniting the classification of cultured and uncultured bacteria and archaea using 16S rRNA gene sequences. Nat Rev Microbiol 12:635–645. https://doi.org/10.1038/nrmicro3330
Yastrebova OV, Plotnikova EG (2020) Phylogenetic diversity of bacteria of the family Micrococcaceae isolated from biotopes with different anthropogenic impact. Bull Perm Univ Biol 4:321–333. https://doi.org/10.17072/1994-9952-2020-4-321-333
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All authors contributed to the study conception and design, including data collection and analysis. The first draft of the manuscript was written by S.Yu. Shchyogolev and L.A. Dykman. All authors commented on initial versions of the manuscript and all authors read and approved the final manuscript.
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Shchyogolev, S.Y., Dykman, L.A., Sokolov, A.O. et al. Quantitative intra- and intergeneric taxonomic relationships among Micrococcaceae strains reveal contradictions in the historical assignments of the strains and indicate the need for species reclassification. Arch Microbiol 206, 165 (2024). https://doi.org/10.1007/s00203-024-03896-7
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DOI: https://doi.org/10.1007/s00203-024-03896-7