Abstract
The Permian Basin is a unique ecosystem located in the southwest of the USA. An unanswered question is whether the bacteria in the Permian Basin adapted to the changing paleomarine environment and survived in the remnants of Permian groundwater. In our previous study, a novel bacterial strain, Permianibacter aggregans HW001T, was isolated from microalgae cultures incubated with Permian Basin waters, and was shown to originate from the Permian Ocean. In this study, strain HW001T was shown to be the representative strain of a novel family, classified as ‘Permianibacteraceae’. The results of molecular dating suggested that the strain HW001T diverged ~ 447 million years ago (mya), which is the early Permian period (~ 250 mya). Genome analysis was used to access its potential energy utilization and biosynthesis capacity. A large number of transporters, carbohydrate-active enzymes and protein-degradation related genes have been annotated in the genome of strain HW001T. In addition, a series of important metabolic pathways, such as peptidoglycan biosynthesis, osmotic stress response system and multifunctional quorum sensing were annotated, which may confer the ability to adapt to various unfavorable environmental conditions. Finally, the evolutionary history of strain HW001T was reconstructed and the horizontal transfer of genes was predicted, indicating that the adaptation of P. aggregans to a changing marine environment depends on the evolution of their metabolic capabilities, especially in signal transmission. In conclusion, the results of this study provide genomic information for revealing the adaptive mechanism of strain HW001T to the changing ancient oceans.
Similar content being viewed by others
Data availability
The genome sequence has been submitted to the GenBank database under BioProject PRJNA526813 and accession number CP037953.
References
Arndt D, Grant JR, Marcu A, Sajed T, Pon A, Liang Y, Wishart DS (2016) PHASTER: a better, faster version of the PHAST phage search tool. Nucleic Acids Res 44:W16–W21
Bein A, Dutton AR (1993) Origin, distribution, and movement of brine in the Permian Basin (USA): a model for displacement of connate brine. Geol Soc Am Bull 105:695–707
Bertelli C, Laird MR, Williams KP, Group SFURC, Lau BY, Hoad G, Winsor GL, Brinkman FS (2017) IslandViewer 4: expanded prediction of genomic islands for larger-scale datasets. Nucleic Acids Res 45:W30–W35
Bouckaert R, Heled J, Kühnert D, Vaughan T, Wu C-H, Xie D, Suchard MA, Rambaut A, Drummond AJ (2014) BEAST 2: a software platform for Bayesian evolutionary analysis. PLoS Comput Biol 10:e1003537
Brissette JL, Russel M, Weiner L, Model P (1990) Phage shock protein, a stress protein of Escherichia coli. Proc Natl Acad Sci USA 87:862–866
Buchfink B, Xie C, Huson DH (2015) Fast and sensitive protein alignment using DIAMOND. Nat Methods 12:59–60
Caspi R, Altman T, Billington R, Dreher K, Foerster H, Fulcher CA, Holland TA, Keseler IM, Kothari A, Kubo A (2014) The MetaCyc database of metabolic pathways and enzymes and the BioCyc collection of pathway/genome databases. Nucleic Acids Res 42:D459–D471
Cheng L, Zou Y, Ding S, Zhang J, Yu X, Cao J, Lu G (2009) Polyamine accumulation in transgenic tomato enhances the tolerance to high temperature stress. J Integr Plant Biol 51:489–499
Cheng C, Dong Z, Han X, Wang H, Jiang L, Sun J, Yang Y, Ma T, Shao C, Wang X, Chen Z, Fang W, Freitag NE, Huang H, Song H (2017) Thioredoxin A is essential for motility and contributes to host infection of Listeria monocytogenes via redox interactions. Front Cell Infect Microbiol 7:287
Chew SC, Yang L (2016) Biofilms. In: Caballero B, Finglas P, Toldrá F (eds) Encyclopedia of food and health. Elsevier, Oxford, pp 407–415
Contreras-Moreira B, Vinuesa P (2013) GET_HOMOLOGUES, a versatile software package for scalable and robust microbial pangenome analysis. Appl Environ Microbiol 79:7696–7701
Csűös M (2010) Count: evolutionary analysis of phylogenetic profiles with parsimony and likelihood. Bioinformatics 26:1910–1912
Darling ACE, Mau B, Blattner FR, Perna NT (2004) Mauve: multiple alignment of conserved genomic sequence with rearrangements. Genome Res 14:1394–1403
David LA, Alm EJ (2011) Rapid evolutionary innovation during an Archaean genetic expansion. Nature 469:93
Denamur E, Matic I (2006) Evolution of mutation rates in bacteria. Mol Microbiol 60:820–827
Didelot X, Wilson D (2015) ClonalFrameML: efficient inference of recombination in whole bacterial genomes. PLoS Comput Biol 11:e1004041
Drula E, Garron ML, Dogan S, Lombard V, Henrissat B, Terrapon N (2022) The carbohydrate-active enzyme database: functions and literature. Nucleic Acids Res 50:D571–D577
Emms DM, Kelly S (2015) Orthofinder: solving fundamental biases in whole genome comparisons dramatically improves orthogroup inference accuracy. Genome Biol 16:157
Falcón LI, Magallón S, Castillo A (2010) Dating the cyanobacterial ancestor of the chloroplast. ISME J 4:777–783
Fernández P, Porrini L, Albanesi D, Abriata LA, Dal Peraro M, De Mendoza D, Mansilla MC (2019) Transmembrane prolines mediate signal sensing and decoding in Bacillus subtilis DesK histidine kinase. mBio 10:e02564-19
Freeman ZN, Dorus S, Waterfield NR (2013) The KdpD/KdpE two-component system: integrating K+ homeostasis and virulence. PLoS Pathog 9:e1003201
Gram L, Grossart H-P, Schlingloff A, Kiørboe T (2002) Possible quorum sensing in marine snow bacteria: production of acylated homoserine lactones by Roseobacter strains isolated from marine snow. Appl Environ Microbiol 68:4111–4116
Gruber N (2008) The marine nitrogen cycle: overview and challenges. Nitrogen Mar Environ 2:1–50
Ho SYW, Duchêne S (2014) Molecular-clock methods for estimating evolutionary rates and timescales. Mol Ecol 2324:5947–5965
Höltje J-V (1998) Growth of the stress-bearing and shape-maintaining murein sacculus of Escherichia coli. Microbiol Mol Biol Rev 62:181–203
Hong Y, Youshao W, Chen F (2013) Archaea dominate ammonia oxidizers in the Permian water ecosystem of midland basin. Microbes Environ 28:396–399
Hua ZS, Qu YN, Zhu Q, Zhou EM, Qi YL, Yin YR, Rao YZ, Tian Y, Li YX, Liu L, Castelle CJ, Hedlund BP, Shu WS, Knight R, Li WJ (2018) Genomic inference of the metabolism and evolution of the archaeal phylum Aigarchaeota. Nat Commun 9:1–11
Huerta-Cepas J, Szklarczyk D, Heller D, Hernández-Plaza A, Forslund SK, Cook H, Mende DR, Letunic I, Rattei T, Jensen LJ, von Mering C, Bork P (2019) eggNOG 5.0: a hierarchical, functionally and phylogenetically annotated orthology resource based on 5090 organisms and 2502 viruses. Nucleic Acids Res 47:D309–D314
Jones P, Binns D, Chang H-Y, Fraser M, Li W, McAnulla C, McWilliam H, Maslen J, Mitchell A, Nuka G, Pesseat S, Quinn AF, Sangrador-Vegas A, Scheremetjew M, Yong S-Y, Lopez R, Hunter S (2014) InterProScan 5: Genome-scale protein function classification. Bioinformatics 30:1236–1240
Katoh K, Standley DM (2014) MAFFT: iterative refinement and additional methods. Methods Mol Biol 1079:131–146
Kim JG, Park SJ, Sinninghe Damsté JS, Schouten S, Rijpstra WIC, Jung WY, Kim SJ, Gwak JH, Hong H, Si OJ, Lee SH, Madsen EL, Rhee SK (2016) Hydrogen peroxide detoxification is a key mechanism for growth of ammonia-oxidizing archaea. Proc Natl Acad Sci USA 113:7888–7893
Kleerebezem M, Crielaard W, Tommassen J (1996) Involvement of stress protein PspA (phage shock protein A) of Escherichia coli in maintenance of the protonmotive force under stress conditions. EMBO J 15:162–171
Knight DR, Elliott B, Chang BJ, Perkins TT, Riley TV (2015) Diversity and evolution in the genome of Clostridium difficile. Clinical Microbiol Rev 28:721–741
Kohl M, Wiese S, Warscheid B (2011) Cytoscape: software for visualization and analysis of biological networks. Methods Mol Biol 696:291–303
Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874
Lagkouvardos I, Joseph D, Kapfhammer M, Giritli S, Horn M, Haller D, Clavel T (2016) IMNGS: a comprehensive open resource of processed 16S rRNA microbial profiles for ecology and diversity studies. Sci Rep 6:33721
Lanfear R, Calcott B, Ho SY, Guindon S (2012) PartitionFinder: combined selection of partitioning schemes and substitution models for phylogenetic analyses. Mol Biol Evol 29:1695–1701
Langenheder S, Comte J, Zha Y, Samad MS, Sinclair L, Eiler A, Lindstrom ES (2016) Remnants of marine bacterial communities can be retrieved from deep sediments in lakes of marine origin. Environ Microbiol Rep 8:479–485
Latasa C, Roux A, Toledo-Arana A, Ghigo J-M, Gamazo C, Penadés JR, Lasa I (2005) BapA, a large secreted protein required for biofilm formation and host colonization of Salmonella enterica serovar Enteritidis. Mol Microbiol 58:1322–1339
Le SQ, Gascuel O (2008) An improved general amino acid replacement matrix. Mol Biol Evol 25:1307–1320
Li L, Stoeckert CJ, Roos DS (2003) OrthoMCL: identification of ortholog groups for eukaryotic genomes. Genome Res 13:2178–2189
Luo H, Csürös M, Hughes AL, Moran MA (2013) Evolution of divergent life history strategies in marine Alphaproteobacteria. mBio 4:e00373-13
Luo ZH, Narsing Rao MP, Chen H, Hua ZS, Li Q, Hedlund BP, Dong ZY, Liu BB, Guo SX, Shu WS, Li WJ (2021) Genomic insights of “Candidatus Nitrosocaldaceae” based on nine new metagenome-assembled genomes, including “Candidatus Nitrosothermus” gen nov. and two new species of “Candidatus Nitrosocaldus.” Front Microbiol 11:3412
Martin DP, Murrell B, Khoosal A, Muhire B (2017) Detecting and analyzing genetic recombination using RDP4. In: Keith JM (ed) Methods in molecular biology. Humana, Totowa, pp 433–460
Mello B (2018) Estimating timetrees with MEGA and the TimeTree resource. Mol Biol Evol 35:2334–2342
Misof B, Liu S, Meusemann K, Peters RS, Donath A, Mayer C, Frandsen PB, Ware J, Flouri T, Beutel RG, Niehuis O, Petersen M, Izquierdo-Carrasco F, Wappler T, Rust J, Aberer AJ, Aspöck U, Aspöck H, Bartel D, Blanke A et al (2014) Phylogenomics resolves the timing and pattern of insect evolution. Science 346:763–767
Moran MA, Buchan A, González JM, Heidelberg JF, Whitman WB, Kiene RP, Henriksen JR, King GM, Belas R, Fuqua C (2004) Genome sequence of Silicibacter pomeroyi reveals adaptations to the marine environment. Nature 432:910
Mori JF, Scott JJ, Hager KW, Moyer CL, Kusel K, Emerson D (2017) Physiological and ecological implications of an iron- or hydrogen-oxidizing member of the Zetaproteobacteria, Ghiorsea bivora, gen. nov., sp. nov. ISME J 11:2624–2636
Nakjang S, Williams TA, Heinz E, Watson AK, Foster PG, Sendra KM, Heaps SE, Hirt RP, Martin Embley T (2013) Reduction and expansion in microsporidian genome evolution: new insights from comparative genomics. Genome Biol Evol 5:2285–2303
Ochman H, Wilson AC (1987) Evolution in bacteria: evidence for a universal substitution rate in cellular genomes. J Mol Evol 26:74–86
Ogilvie BG, Rutter M, Nedwell DB (1997) Selection by temperature of nitrate-reducing bacteria from estuarine sediments: species composition and competition for nitrate. FEMS Microbiol Ecol 23:11–22
Oliveira PH, Touchon M, Cury J, Rocha EP (2017) The chromosomal organization of horizontal gene transfer in bacteria. Nat Commun 8:1–11
Puigbò P, Bravo IG, Garcia-Vallve S (2008) CAIcal: a combined set of tools to assess codon usage adaptation. Biol Direct 3:38
Rambaut A (2018) Figtree, a graphical viewer of phylogenetic trees, version 1.4. 4. Institute of evolutionary biology, University of Edinburgh
Rambaut A, Drummond AJ, Xie D, Baele G, Suchard MA (2018) Posterior summarization in Bayesian phylogenetics using Tracer 1.7. Syst Biol 67:901–904
Rand L, Hinds J, Springer B, Sander P, Buxton RS, Davis EO (2003) The majority of inducible DNA repair genes in Mycobacterium tuberculosis are induced independently of RecA. Mol Microbiol 50:1031–1042
Revelle WR (2013) psych: procedures for personality and psychological research. Available http://CRAN.R-project.org/package=psych Version = 1.3.10. Accessed 20 Dec 2013
Sanderson MJ (2003) r8s: inferring absolute rates of molecular evolution and divergence times in the absence of a molecular clock. Bioinformatics 19:301–302
Seemann T (2014) Prokka: rapid prokaryotic genome annotation. Bioinformatics 30:2068–2069
Stamatakis A (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30:1312–1313
Sun H, Xiao Y, Gao Y, Zhang G, Casey JF, Shen Y (2018) Rapid enhancement of chemical weathering recorded by extremely light seawater lithium isotopes at the Permian-Triassic boundary. Proc Natl Acad Sci USA 115:3782–3787
Team RC (2013) R: A language and environment for statistical computing. Available http://www.R-project.org. Accessed 2 Feb 2013
Toulza E, Tagliabue A, Blain S, Piganeau G (2012) Analysis of the Global Ocean Sampling (GOS) project for trends in iron uptake by surface ocean microbes. PLoS ONE 7:e30931
Troxell B, Hassan HM (2013) Transcriptional regulation by Ferric Uptake Regulator (Fur) in pathogenic bacteria. Front Cell Infect Microbiol 3:59
Wang H, Laughinghouse HD, Anderson MA, Chen F, Willliams E, Place AR, Zmora O, Zohar Y, Zheng T, Hill RT (2012) Novel bacterial isolate from Permian groundwater, capable of aggregating potential biofuel-producing microalga Nannochloropsis oceanica IMET1. Appl Environ Microbiol 78:1445–1453
Wang H, Zheng T, Hill RT, Hu X (2014) Permianibacter aggregans gen. nov., sp. nov., a bacterium of the family Pseudomonadaceae capable of aggregating potential biofuel-producing microalgae. Int J Syst Evol Microbiol 64:3503–3507
Wright WR (2011) Pennsylvanian paleodepositional evolution of the greater Permian Basin, Texas and New Mexico: depositional systems and hydrocarbon reservoir analysis. AAPG Bull 95:1525–1555
Xiao R, Zheng Y (2016) Overview of microalgal extracellular polymeric substances (EPS) and their applications. Biotechnol Adv 34:1225–1244
Xiao R, Yang X, Li M, Li X, Wei Y, Cao M, Ragauskas A, Thies M, Ding J, Zheng Y (2018) Investigation of composition, structure and bioactivity of extracellular polymeric substances from original and stress-induced strains of Thraustochytrium striatum. Carbohyd Polym 195:515–524
Yang Z (1996) Among-site rate variation and its impact on phylogenetic analyses. Trends Ecol Evol 11:367–372
Yarza P, Yilmaz P, Pruesse E, Glöckner FO, Ludwig W, Schleifer K-H, 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
Yin S, Chen D, Chen L, Edis R (2002) Dissimilatory nitrate reduction to ammonium and responsible microorganisms in two Chinese and Australian paddy soils. Soil Biol Biochemi 34:1131–1137
Yoon S-H, Ha S-M, Lim J, Kwon S, Chun J (2017) A large-scale evaluation of algorithms to calculate average nucleotide identity. Ant v Leeuwenhoek 110:1281–1286
Zhaxybayeva O, Swithers KS, Lapierre P, Fournier GP, Bickhart DM, DeBoy RT, Nelsond KE, Nesbøe CL, Doolittlea WF, Gogarten JP, Noll KM (2009) On the chimeric nature, thermophilic origin, and phylogenetic placement of the Thermotogales. Proc Natl Acad Sci USA 106:5865–5870
Zhu Q, Kosoy M, Dittmar K (2014) HGTector: an automated method facilitating genome-wide discovery of putative horizontal gene transfers. BMC Genomics 15:1–18
Acknowledgements
Funding for this study was provided by the Key Special Project for Introduced Talents Team of Southern Marine Science and Engineering Guangdong Laboratory (Guangzhou) (GML2019ZD0606), National Natural Science Foundation of China (92051118), Guangdong Science and Technology Department (2019A1515011139), and 2020 Li Ka Shing Foundation (LKSF) Cross-Disciplinary Research Grant (2020LKSFG07A).
Author information
Authors and Affiliations
Contributions
HW and RTH conceived and designed the experiments; SZ performed the experiments and drafted the manuscript; HW, RTH, and SZ revised the manuscript; HW supervised the project. The final manuscript was approved by all of the authors.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that there is no conflict of interest.
Animal and human rights statement
This article does not contain any studies performed with human and animals.
Additional information
Edited by Jiamei Li.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Zhang, S., Hill, R.T. & Wang, H. Genomic characterization and molecular dating of the novel bacterium Permianibacter aggregans HW001T, which originated from Permian ground water. Mar Life Sci Technol 5, 12–27 (2023). https://doi.org/10.1007/s42995-023-00164-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s42995-023-00164-3