Original Article

Core genome expansion in Brevibacterium across marine provinces reveals genomic footprint for long-term marine adaptation

Abstract

Background and Objectives: Actinobacteria are ubiquitous across diverse environmental niches. Brevibacterium strains within this phylum are widely distributed in both marine and terrestrial ecosystems worldwide. Marine environments are defined by distinct physicochemical properties—high salinity, alkaline pH, fluctuating O2 levels, and dynamic nutrient availability—which set them apart from terrestrial habitats. The broad ecological range of Brevibacterium strains raises questions about genome-encoded metabolic features that have evolved to adapt in marine environments.
Materials and Methods: Genomics of Brevibacterium strains from various marine provinces was analyzed, focusing on core genome and pan-genome structure.
Results: Core genome and pan-genome derived phylograms reveal a distinct polyphyletic origin of marine strains, as evidenced by their phylogenetic proximity despite diverse species affiliations. Only 1.16% of gene clusters from the total nonredundant gene repertoire were part of the core genome. Core genome size is shaped by geographical distribution. Notably, when strains from localized regions are analyzed, the core genome expands, indicating specialized functional requirements of additional genes within that environment. In marine isolates, the core genome includes genes involved in nutrient uptake, osmoregulation, and resistance to sediment genotoxicity. Additionally, a marine province-specific core genome analysis reveals genomic adaptations essential for acclimatization across different environments, regardless of species-level
taxonomy.
Conclusion: Microbial genome evolution is shaped by ecological niche differentiation. The emergence and spread of habitats driven by tectonic plate movements may contribute to province-specific genomic divergence in Brevibacterium. This hypothesis merits further investigation, particularly as genomic data from deeper, geologically stable environments such as marine sediments become more accessible.

1. Ward AC, Bora N. Diversity and biogeography of marine actinobacteria. Curr Opin Microbiol 2006; 9: 279-286.
2. Valverde A, Tuffin M, Cowan DA. Biogeography of bacterial communities in hot springs: a focus on the actinobacteria. Extremophiles 2012; 16: 669-679.
3. Mohammadipanah F, Wink J. Actinobacteria from arid and desert Habitats: Diversity and Biological activity. Front Microbiol 2016; 6: 1541.
4. Neuenschwander SM, Ghai R, Pernthaler J, Salcher MM. Microdiversification in genome-streamlined ubiquitous freshwater Actinobacteria. ISME J 2018; 12: 185-198.
5. Deng T, Lu H, Qian Y, Chen X, Yang X, Guo J, et al. Brevibacterium rongguiense sp. nov., isolated from freshwater sediment. Int J Syst Evol Microbiol 2020; 70: 5205-5210.
6. Chen P, Zhang L, Wang J, Ruan J, Han X, Huang Y. Brevibacterium sediminis sp. nov., isolated from deep-sea sediments from the Carlsberg and Southwest Indian Ridges. Int J Syst Evol Microbiol 2016; 66: 5268-5274.
7. Jung MS, Quan XT, Siddiqi MZ, Liu Q, Kim SY, Wee JH, et al. Brevibacterium anseongense sp. nov., isolated from soil of ginseng field. J Microbiol 2018; 56: 706-712.
8. Belov AA, Cheptsov VS, Vorobyova EA, Manucharova NA, Ezhelev ZS. Stress-tolerance and taxonomy of culturable bacterial communities isolated from a Central Mojave Desert soil sample. Geosciences 2019; 9: 166.
9. Pei S, Xie F, Niu S, Ma L, Zhang R, Zhang G. Brevibacterium profundi sp. nov., isolated from deep-sea sediment of the Western Pacific Ocean. Int J Syst Evol Microbiol 2020; 70: 5818-5823.
10. Zhao J, Shakir Y, Deng Y, Zang Y. Use of modified ichip for the cultivation of thermo-tolerant microorganisms from the hot spring. BMC Microbiol 2023; 23: 56.
11. Collins MD. The genus Brevibacterium. Prokaryotes 2006; 3: 1013-1019.
12. Hoshino T, Doi H, Uramoto GI, Wörmer L, Adhikari RR, Xiao N, et al. Global diversity of microbial communities in marine sediment. Proc Natl Acad Sci U S A 2020; 117: 27587-27597.
13. Dmitrijeva M, Tackmann J, Matias Rodrigues JF, Huerta-Cepas J, Coelho LP, von Mering C. A global survey of prokaryotic genomes reveals the eco-evolutionary pressures driving horizontal gene transfer. Nat Ecol Evol 2024; 8: 986-998.
14. Arnold BJ, Huang IT, Hanage WP. Horizontal gene transfer and adaptive evolution in bacteria. Nat Rev Microbiol 2022; 20: 206-218.
15. Lee SD. Brevibacterium marinum sp. nov., isolated from seawater. Int J Syst Evol Microbiol 2008; 58: 500-504.
16. Pei S, Niu S, Xie F, Wang W, Zhang S, Zhang G. Brevibacterium limosum sp. nov., Brevibacterium pigmenatum sp. nov., and Brevibacterium atlanticum sp. nov., three novel dye decolorizing actinobacteria isolated from ocean sediments. J Microbiol 2021; 59: 898-910.
17. Bhadra B, Raghukumar C, Pindi PK, Shivaji S. Brevibacterium oceani sp. nov., isolated from deep-sea sediment of the Chagos Trench, Indian Ocean. Int J Syst Evol Microbiol 2008; 58: 57-60.
18. Pham NP, Layec S, Dugat-Bony E, Vidal M, Irlinger F, Monnet C. Comparative genomic analysis of Brevibacterium strains: insights into key genetic determinants involved in adaptation to the cheese habitat. BMC Genomics 2017; 18: 955.
19. Levesque S, de Melo AG, Labrie SJ, Moineau S. Mobilome of Brevibacterium aurantiacum sheds light on its genetic diversity and its adaptation to smear-ripened cheeses. Front Microbiol 2019; 10: 1270.
20. Cumsille A, Serna-Cardona N, González V, Claverías F, Undabarrena A, Molina V, et al. Exploring the biosynthetic gene clusters in Brevibacterium: a comparative genomic analysis of diversity and distribution. BMC Genomics 2023; 24: 622.
21. Sarkar J, Mondal M, Bhattacharya S, Dutta S, Chatterjee S, Mondal N, et al. Extremely oligotrophic and complex-carbon-degrading microaerobic bacteria from Arabian Sea oxygen minimum zone sediments. Arch Microbiol 2024; 206: 179.
22. Meier-Kolthoff JP, Göker M. TYGS is an automated high-throughput platform for state-of-the-art genome-based taxonomy. Nat Commun 2019; 10: 2182.
23. Chaudhari NM, Gupta VK, Dutta C. BPGA- an ultra-fast pan-genome analysis pipeline. Sci Rep 2016; 6: 24373.
24. Edgar RC. Search and clustering orders of magnitude faster than BLAST. Bioinformatics 2010; 26: 2460-2461.
25. Edgar RC. MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics 2004; 5: 113.
26. Vos RA, Caravas J, Hartmann K, Jensen MA, Miller C. BIO::Phylo-phyloinformatic analysis using perl. BMC Bioinformatics 2011; 12: 63.
27. Jain C, Rodriguez-R LM, Phillippy AM, Konstantinidis KT, Aluru S. High throughput ANI analysis of 90K prokaryotic genomes reveals clear species boundaries. Nat Commun 2018; 9: 5114.
28. Cantalapiedra CP, Hernández-Plaza A, Letunic I, Bork P, Huerta-Cepas J. eggNOG-mapper v2: Functional Annotation, Orthology Assignments, and Domain Prediction at the Metagenomic Scale. Mol Biol Evol 2021; 38: 5825-5829.
29. Liu M, Siezen RJ, Nauta A. In silico prediction of horizontal gene transfer events in Lactobacillus bulgaricus and Streptococcus thermophilus reveals protocooperation in yogurt manufacturing. Appl Environ Microbiol 2009; 75: 4120-4129.
30. Ravenhall M, Škunca N, Lassalle F, Dessimoz C. Inferring horizontal gene transfer. PLoS Comput Biol 2015; 11(5): e1004095.
31. D'Hondt S, Spivack AJ, Pockalny R, Ferdelman TG, Fischer JP, Kallmeyer J, et al. Subseafloor sedimentary life in the South Pacific Gyre. Proc Natl Acad Sci U S A 2009; 106: 11651-11656.
32. D’hondt S, Inagaki F, Zarikian CA, Abrams LJ, Dubois N, Engelhardt T, et al. Presence of oxygen and aerobic communities from sea floor to basement in deep-sea sediments. Nat Geosci 2015; 8: 299-304.
33. Sarkar J, Mondal N, Mandal S, Chatterjee S, Ghosh W (2022). Deep Subsurface Microbiomes of the Marine Realm. Systems Biogeochemistry of Major Marine Biomes. pp109-131.
34. Griffiths JR, Kadin M, Nascimento FJ, Tamelander T, Törnroos A, Bonaglia S, et al. The importance of benthic–pelagic coupling for marine ecosystem functioning in a changing world. Glob Chang Biol 2017; 23: 2179-2196.
35. Kallmeyer J, Pockalny R, Adhikari RR, Smith DC, D'Hondt S. Global distribution of microbial abundance and biomass in subseafloor sediment. Proc Natl Acad Sci U S A 2012; 109: 16213-16216.
36. Torres-Beltrán M, Vargas-Gastélum L, Magdaleno-Moncayo D, Riquelme M, Herguera-García JC, Prieto-Davó A, et al. The metabolic core of the prokaryotic community from deep-sea sediments of the southern Gulf of Mexico shows different functional signatures between the continental slope and abyssal plain. PeerJ 2021; 9: e12474.
37. Batzke A, Engelen B, Sass H, Cypionka H. Phylogenetic and physiological diversity of cultured deep-biosphere bacteria from Equatorial Pacific Ocean and Peru Margin sediments. Geomicrobiol J 2007; 24: 261-273.
38. Bhattacharya S, Roy C, Mandal S, Sarkar J, Rameez MJ, Mondal N, et al. Aerobic microbial communities in the sediments of a marine oxygen minimum zone. FEMS Microbiol Lett 2020; 367: fnaa157.
39. Shoemaker WR, Jones SE, Muscarella ME, Behringer MG, Lehmkuhl BK, Lennon JT. Microbial population dynamics and evolutionary outcomes under extreme energy limitation. Proc Natl Acad Sci U S A 2021; 118(33): e2101691118.
40. Alonso-Sáez L, Gasol JM. Seasonal variations in the contributions of different bacterial groups to the uptake of low-molecular-weight compounds in northwestern Mediterranean coastal waters. Appl Environ Microbiol 2007; 73: 3528-3535.
41. Fernandes L, Garg A, Borole DV. Amino acid biogeochemistry and bacterial contribution to sediment organic matter along the western margin of the Bay of Bengal. Deep-Sea Res I: Oceanogr Res Pap 2014; 83: 81-92.
42. Choi H, Choi B, Chikaraishi Y, Takano Y, Kim H, Lee K, et al. Microbial alteration in marine sediments: Insights from compound-specific isotopic compositions of amino acids in subseafloor environments. Front Mar Sci 2022; 9: 10.3389/fmars.2022.1030669.
43. Yancey PH. Compatible and Counteracting Solutes: Protecting Cells from the Dead Sea to the Deep Sea. Sci Prog 2004; 87: 1-24.
44. Wood JM, Bremer E, Csonka LN, Kraemer R, Poolman B, van der Heide T, et al. Osmosensing and osmoregulatory compatible solute accumulation by bacteria. Comp Biochem Physiol A Mol Integr Physiol 2001; 130: 437-460.
45. Welsh DT. Ecological significance of compatible solute accumulation by micro-organisms: from single cells to global climate. FEMS Microbiol Rev 2000; 24: 263-290.
46. Kammann U, Riggers JC, Theobald N, Steinhart H. Genotoxic potential of marine sediments from the North Sea. Mutat Res 2000; 467: 161-168.
47. Dai X, Zhu M. High Osmolarity Modulates Bacterial cell size through reducing initiation volume in Escherichia coli. mSphere 2018; 3(5): e00430-18.
48. Dupuy P, Sauviac L, Bruand C. Stress-inducible NHEJ in bacteria: function in DNA repair and acquisition of heterologous DNA. Nucleic Acids Res 2019; 47: 1335-1349.
49. Mathivanan K, Chandirika JU, Vinothkanna A, Yin H, Liu X, Meng D. Bacterial adaptive strategies to cope with metal toxicity in the contaminated environment – A review. Ecotoxicol Environ Saf 2021; 226: 112863.
50. Pedraza-Reyes M, Abundiz-Yañez K, Rangel-Mendoza A, Martínez LE, Barajas-Ornelas RC, Cuéllar-Cruz M, et al. Bacillus subtilis stress-associated mutagenesis and developmental DNA repair. Microbiol Mol Biol Rev 2024; 88(2): e0015823.
51. Hwang S, Choe D, Yoo M, Cho S, Kim SC, Cho S, et al. Peptide transporter CstA imports pyruvate in Escherichia coli K-12. J Bacteriol 2018; 200(7): e00771-17.
52. Mohsin H, Shafique M, Zaid M, Rehman Y. Microbial biochemical pathways of arsenic biotransformation and their application for bioremediation. Folia Microbiol (Praha) 2023; 68: 507-535.
53. Zhang Y, Gross CA. Cold shock response in Bacteria. Annu Rev Genet 2021; 55: 377-400.
54. Mandal S, Bhattacharya S, Roy C, Ramez MJ, Sarkar j, Mapder T, et al. Cryptic roles of tetrathionate in the sulfur cycle of marine sediments: microbial drivers and indicators. Biogeosciences 2020; 17: 4611-4631.
Files
IssueVol 17 No 6 (2025) QRcode
SectionOriginal Article(s)
DOI https://doi.org/10.18502/ijm.v17i6.20358
Keywords
Actinobacteria Biological adaptation Genome Marine ecology Horizontal gene transfer

Rights and permissions
Creative Commons License This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.
How to Cite
1.
Sarkar J. Core genome expansion in Brevibacterium across marine provinces reveals genomic footprint for long-term marine adaptation. Iran J Microbiol. 2025;17(6):912-928.