Skip to main content
Log in

Characteristics and adaptability of Flavobacterium panici BSSL-CR3 in tidal flat revealed by comparative genomic and enzymatic analysis

  • Original Paper
  • Published:
Archives of Microbiology Aims and scope Submit manuscript

Abstract

Tidal flat microbes play an important ecological role by removing organic pollutants and providing an energy source. However, bacteria isolated from tidal flats and their genomes have been scarcely reported, making it difficult to elucidate which genes and pathways are potentially involved in the above roles. In this study, strain BSSL-CR3, the third reported species among the tidal flat Flavobacterium was analyzed using whole-genome sequencing to investigate its adaptability and functionality in tidal flats. BSSL-CR3 is comprised of a circular chromosome of 5,972,859 bp with a GC content of 33.84%. Genome annotation and API ZYM results showed that BSSL-CR3 has a variety of secondary metabolic gene clusters and enzyme activities including α-galactosidase. BSSL-CR3 had more proteins with a low isoelectric point (pI) than terrestrial Flavobacterium strains, and several genes related to osmotic regulation were found in the genomic island (GI). Comparative genomic analysis with other tidal flat bacteria also revealed that BSSL-CR3 had the largest number of genes encoding Carbohydrate Active EnZymes (CAZymes) which are related to algae degradation. This study will provide insight into the adaptability of BSSL-CR3 to the tidal flats and contribute to facilitating future comparative analysis of bacteria in tidal flats.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Data availability

The complete genome sequence of F. panici BSSL-CR3 has been deposited in GenBank under the accession number CP100437.

References

  • Abdel-Mageed WM et al (2020) Whole genome sequencing of four bacterial strains from South Shetland Trench revealing biosynthetic and environmental adaptation gene clusters. Mar Genomics 54:100782

    Article  Google Scholar 

  • Aguado-Santacruz GA, Moreno-Gómez B, Jiménez-Francisco B, García-Moya E, Preciado-Ortiz RE (2012) Impact of the microbial siderophores and phytosiderophores on the iron assimilation by plants: a synthesis. Rev Fitotec Mex 35:9–21

    Google Scholar 

  • Aruldass CA, Dufossé L, Ahmad WA (2018) Current perspective of yellowish-orange pigments from microorganisms-a review. J Clean Prod 180:168–182

    Article  CAS  Google Scholar 

  • Bae SS, Kim MR, Jung Y, Yang S-H, Kwon KK, Baek K (2018) Flavobacterium sediminis sp. nov., a starch-degrading bacterium isolated from tidal flat sediment. Int J Syst Evol Microbiol 68:3886–3891

    Article  CAS  Google Scholar 

  • Barbeyron T et al (2016) Habitat and taxon as driving forces of carbohydrate catabolism in marine heterotrophic bacteria: example of the model algae-associated bacterium Zobellia galactanivorans DsijT. Environ Microbiol 18:4610–4627

    Article  CAS  Google Scholar 

  • Bertelli C, Laird M, Williams K, Simon Fraser University Research Computing Group; Lau BY, Hoad G, Winsor GL, Brinkman FSL (2017) IslandViewer 4: expanded prediction of genomic islands for larger-scale datasets. Nucleic Acids Res 45:W30-35

    Article  Google Scholar 

  • Bissett A, Bowman JP, Burke CM (2008) Flavobacterial response to organic pollution. Aquat Microb Ecol 51:31–43

    Article  Google Scholar 

  • Blin K et al (2021) antiSMASH 6.0: improving cluster detection and comparison capabilities. Nucleic Acids Res 49:W29–W35

    Article  CAS  Google Scholar 

  • Boiteau RM et al (2016) Siderophore-based microbial adaptations to iron scarcity across the eastern Pacific Ocean. Proc Natl Acad Sci 113:14237–14242

    Article  CAS  Google Scholar 

  • Bruhn A et al (2011) Bioenergy potential of Ulva lactuca: biomass yield, methane production and combustion. Biores Technol 102:2595–2604

    Article  CAS  Google Scholar 

  • Cantalapiedra CP, Hernández-Plaza A, Letunic I, Bork P, Huerta-Cepas J (2021) eggNOG-mapper v2: functional annotation, orthology assignments, and domain prediction at the metagenomic scale. Mol Biol Evol 38:5825–5829

    Article  CAS  Google Scholar 

  • Capella-Gutiérrez S, Silla-Martínez JM, Gabaldón T (2009) trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics 25:1972–1973

    Article  Google Scholar 

  • Chen M-Y et al (2021) Comparative genomics reveals insights into cyanobacterial evolution and habitat adaptation. ISME J 15:211–227

    Article  Google Scholar 

  • Chun J et al (2018) Proposed minimal standards for the use of genome data for the taxonomy of prokaryotes. Int J Syst Evol Microbiol 68:461–466

    Article  CAS  Google Scholar 

  • Couvin D et al (2018) CRISPRCasFinder, an update of CRISRFinder, includes a portable version, enhanced performance and integrates search for Cas proteins. Nucleic Acids Res 46:W246–W251. https://doi.org/10.1093/nar/gky425

    Article  CAS  Google Scholar 

  • Danecek P et al (2021) Twelve years of SAMtools and BCFtools. GigaScience. https://doi.org/10.1093/gigascience/giab008

    Article  Google Scholar 

  • Debnath SC et al (2019) Flavobacterium sharifuzzamanii sp. nov., isolated from the sediments of the East China Sea. Curr Microbiol 76:297–303. https://doi.org/10.1007/s00284-018-1609-7

    Article  CAS  Google Scholar 

  • Decostere A, Haesebrouck F, Devriese L (1998) Characterization of four Flavobacterium columnare (Flexibacter columnaris) strains isolated from tropical fish. Vet Microbiol 62:35–45

    Article  CAS  Google Scholar 

  • Delcher AL, Salzberg SL, Phillippy AM (2003) Using MUMmer to identify similar regions in large sequence sets. Curr Protoc Bioinform. https://doi.org/10.1002/0471250953.bi1003s00

    Article  Google Scholar 

  • Fu Y et al (2011) Flavobacterium beibuense sp. nov., isolated from marine sediment. Int J Syst Evol Microbiol 61:205–209

    Article  CAS  Google Scholar 

  • Green DH, Shenoy DM, Hart MC, Hatton AD (2011) Coupling of dimethylsulfide oxidation to biomass production by a marine flavobacterium. Appl Environ Microbiol 77:3137–3140

    Article  CAS  Google Scholar 

  • Hahnke RL et al (2015) High quality draft genome sequence of Flavobacterium rivuli type strain WB 3.3-2T (DSM 21788T), a valuable source of polysaccharide decomposing enzymes. Stand Genomic Sci 10:1–16

    Article  Google Scholar 

  • Han J-H, Shim H, Shin J-H, Kim KS (2015) Antagonistic activities of Bacillus spp. strains isolated from tidal flat sediment towards anthracnose pathogens Colletotrichum acutatum and C. gloeosporioides in South Korea. Plant Pathol J 31:165

    Article  Google Scholar 

  • Higashioka Y, Kojima H, Watanabe M, Fukui M (2013) Desulfatitalea tepidiphila gen. nov., sp. nov., a sulfate-reducing bacterium isolated from tidal flat sediment. Int J Syst Evol Microbiol 63:761–765

    Article  CAS  Google Scholar 

  • Hoang DT, Chernomor O, Von Haeseler A, Minh BQ, Vinh LS (2018) UFBoot2: improving the ultrafast bootstrap approximation. Mol Biol Evol 35:518–522

    Article  CAS  Google Scholar 

  • Huerta-Cepas J et al (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

    Article  CAS  Google Scholar 

  • Humphry DR, George A, Black GW, Cummings SP (2001) Flavobacterium frigidarium sp. nov., an aerobic, psychrophilic, xylanolytic and laminarinolytic bacterium from Antarctica. Int J Syst Evol Microbiol 51:1235–1243

    Article  CAS  Google Scholar 

  • Hunt M, Silva ND, Otto TD, Parkhill J, Keane JA, Harris SR (2015) Circlator: automated circularization of genome assemblies using long sequencing reads. Genome Biol 16:1–10

    Article  Google Scholar 

  • Jin HM, Kim KH, Jeon CO (2015) Alteromonas naphthalenivorans sp. nov., a polycyclic aromatic hydrocarbon-degrading bacterium isolated from tidal-flat sediment. Int J Syst Evol Microbiol 65:4208–4214

    Article  CAS  Google Scholar 

  • Kalyaanamoorthy S, Minh BQ, Wong TK, Von Haeseler A, Jermiin LS (2017) ModelFinder: fast model selection for accurate phylogenetic estimates. Nat Methods 14:587–589

    Article  CAS  Google Scholar 

  • Kämpfer P et al (2020) Flavobacterium panici sp. nov. isolated from the rhizosphere of the switchgrass Panicum virgatum. Int J Syst Evol Microbiol 70:5824–5831

    Article  Google Scholar 

  • Kim B-Y et al (2006) Flavobacterium daejeonense sp. nov. and Flavobacterium suncheonense sp. nov., isolated from greenhouse soils in Korea. Int J Syst Evol Microbiol 56:1645–1649

    Article  CAS  Google Scholar 

  • Kim J-D, Kim J-Y, Park J-K, Lee C-G (2009) Selective control of the Prorocentrum minimum harmful algal blooms by a novel algal-lytic bacterium Pseudoalteromonas haloplanktis AFMB-008041. Mar Biotechnol 11:463–472

    Article  CAS  Google Scholar 

  • Kim S-G, Pheng S, Lee Y-J, Eom MK, Shin D-H (2016) Agarivorans aestuarii sp. nov., an agar-degrading bacterium isolated from a tidal flat. Int J Syst Evol Microbiol 66:3119–3124

    Article  CAS  Google Scholar 

  • Kim I, Kim J, Chhetri G, Seo T (2019) Flavobacterium humi sp. nov., a flexirubin-type pigment producing bacterium, isolated from soil. J Microbiol 57:1079–1085. https://doi.org/10.1007/s12275-019-9350-x

    Article  CAS  Google Scholar 

  • Kirchman DL (2002) The ecology of Cytophaga-Flavobacteria in aquatic environments. FEMS Microbiol Ecol 39:91–100

    CAS  Google Scholar 

  • Koh C-H, Khim JS (2014) The Korean tidal flat of the Yellow Sea: physical setting, ecosystem and management. Ocean Coast Manag 102:398–414

    Article  Google Scholar 

  • Kolmogorov M, Yuan J, Lin Y, Pevzner PA (2019) Assembly of long, error-prone reads using repeat graphs. Nat Biotechnol 37:540–546

    Article  CAS  Google Scholar 

  • Kong N et al (2017) Automation of PacBio SMRTbell NGS library preparation for bacterial genome sequencing. Stand Genomic Sci 12:1–10

    Article  Google Scholar 

  • Kustka AB, Jones BM, Hatta M, Field MP, Milligan AJ (2015) The influence of iron and siderophores on eukaryotic phytoplankton growth rates and community composition in the Ross Sea. Mar Chem 173:195–207

    Article  CAS  Google Scholar 

  • Laurens LM et al (2017) Development of algae biorefinery concepts for biofuels and bioproducts; a perspective on process-compatible products and their impact on cost-reduction. Energy Environ Sci 10:1716–1738

    Article  CAS  Google Scholar 

  • Lee Y, Jeon CO (2018) Flavobacterium alvei sp. nov., isolated from a freshwater river. Int J Syst Evol Microbiol 68:1919–1924. https://doi.org/10.1099/ijsem.0.002768

    Article  CAS  Google Scholar 

  • Lee I, Chalita M, Ha S-M, Na S-I, Yoon S-H, Chun J (2017) ContEst16S: an algorithm that identifies contaminated prokaryotic genomes using 16S RNA gene sequences. Int J Syst Evol Microbiol 67:2053–2057. https://doi.org/10.1099/ijsem.0.001872

    Article  CAS  Google Scholar 

  • Lee PA et al (2022) Complete genome sequence of Flavobacterium sediminilitoris YSM-43T, isolated from tidal sediment in Yeosu. Microbiol Resour Announc 11:e0005422. https://doi.org/10.1128/mra.00054-22

    Article  CAS  Google Scholar 

  • Li D-D et al (2017) Flavobacterium arcticum sp. nov., isolated from Arctic seawater. Int J Syst Evol Microbiol 67:1070–1074

    Article  CAS  Google Scholar 

  • Li Y et al (2019) Complete genome sequence of Flavobacterium arcticum SM1502T, exhibiting adaption to the Arctic marine salty environment. Mar Genomics 47:100670

    Article  Google Scholar 

  • Li W et al (2021) RefSeq: expanding the prokaryotic genome annotation pipeline reach with protein family model curation. Nucleic Acids Res 49:D1020–D1028. https://doi.org/10.1093/nar/gkaa1105

    Article  CAS  Google Scholar 

  • Lidbury ID, Murrell JC, Chen Y (2015) Trimethylamine and trimethylamine N-oxide are supplementary energy sources for a marine heterotrophic bacterium: implications for marine carbon and nitrogen cycling. ISME J 9:760–769

    Article  CAS  Google Scholar 

  • Lim C-S et al (2011) Flavobacterium chungbukense sp. nov., isolated from soil. Int J Syst Evol Microbiol 61:2734–2739

    Article  CAS  Google Scholar 

  • Liu B, Zheng D, Zhou S, Chen L, Yang J (2021) VFDB 2022: a general classification scheme for bacterial virulence factors. Nucleic Acids Res 50:D912–D917. https://doi.org/10.1093/nar/gkab1107

    Article  CAS  Google Scholar 

  • Lombard V, Golaconda Ramulu H, Drula E, Coutinho PM, Henrissat B (2014) The carbohydrate-active enzymes database (CAZy) in 2013. Nucleic Acids Res 42:D490–D495

    Article  CAS  Google Scholar 

  • Luo Y, Ruan L-F, Zhao C-M, Wang C-X, Peng D-H, Sun M (2011) Validation of the intact zwittermicin A biosynthetic gene cluster and discovery of a complementary resistance mechanism in Bacillus thuringiensis. Antimicrob Agents Chemother 55:4161–4169

    Article  CAS  Google Scholar 

  • Mann AJ et al (2013) The genome of the alga-associated marine flavobacterium Formosa agariphila KMM 3901T reveals a broad potential for degradation of algal polysaccharides. Appl Environ Microbiol 79:6813–6822

    Article  CAS  Google Scholar 

  • Manni M, Berkeley MR, Seppey M, Simão FA, Zdobnov EM (2021) BUSCO update: novel and streamlined workflows along with broader and deeper phylogenetic coverage for scoring of eukaryotic, prokaryotic, and viral genomes. Mol Biol Evol 38:4647–4654

    Article  CAS  Google Scholar 

  • Math RK et al (2012) Comparative genomics reveals adaptation by Alteromonas sp. SN2 to marine tidal-flat conditions: cold tolerance and aromatic hydrocarbon metabolism. PLoS ONE 7:e35784

    Article  CAS  Google Scholar 

  • McCammon SA, Bowman JP (2000) Taxonomy of Antarctic Flavobacterium species: description of Flavobacterium gillisiae sp. nov., Flavobacterium tegetincola sp. nov., and Flavobacterium xanthum sp. nov., nom. rev. and reclassification of [Flavobacterium] salegens as Salegentibacter salegens gen. nov., comb. nov. Int J Syst Evol Microbiol 50:1055–1063

    Article  CAS  Google Scholar 

  • Meier-Kolthoff JP, Carbasse JS, Peinado-Olarte RL, Göker M (2021) TYGS and LPSN: a database tandem for fast and reliable genome-based classification and nomenclature of prokaryotes. Nucleic Acids Res. https://doi.org/10.1093/nar/gkab902

    Article  Google Scholar 

  • Menon RR, Kumari S, Viver T, Rameshkumar N (2020) Flavobacterium pokkalii sp nov, a novel plant growth promoting native rhizobacteria isolated from pokkali rice grown in coastal saline affected agricultural regions of southern India, Kerala. Microbiol Res 240:126533

    Article  CAS  Google Scholar 

  • Minh BQ et al (2020) IQ-TREE 2: new models and efficient methods for phylogenetic inference in the genomic era. Mol Biol Evol 37:1530–1534

    Article  CAS  Google Scholar 

  • Moya G et al (2017) Flavobacterium hibisci sp. nov., isolated from the rhizosphere of Hibiscus syriacus L. Int J Syst Evol Microbiol 67:537–542

    Article  CAS  Google Scholar 

  • Naysim L, Kang HJ, Jeon CO et al (2014) Zhongshania aliphaticivorans sp. nov., an aliphatic hydrocarbon-degrading bacterium isolated from marine sediment, and transfer of Spongiibacter borealis Jang et al. 2011 to the genus Zhongshania as Zhongshania borealis comb. nov. Int J Syst Evol Microbiol 64:3768–3774

    Article  Google Scholar 

  • Ozturk S, Aslim B (2010) Modification of exopolysaccharide composition and production by three cyanobacterial isolates under salt stress. Environ Sci Pollut Res 17:595–602

    Article  CAS  Google Scholar 

  • Parks DH, Imelfort M, Skennerton CT, Hugenholtz P, Tyson GW (2015) CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes. Genome Res 25:1043–1055

    Article  CAS  Google Scholar 

  • Pedler BE, Aluwihare LI, Azam F (2014) Single bacterial strain capable of significant contribution to carbon cycling in the surface ocean. Proc Natl Acad Sci 111:7202–7207

    Article  CAS  Google Scholar 

  • Pritchard L, Glover RH, Humphris S, Elphinstone JG, Toth IK (2016) Genomics and taxonomy in diagnostics for food security: soft-rotting enterobacterial plant pathogens. Anal Methods 8:12–24

    Article  Google Scholar 

  • Pruesse E, Peplies J, Glöckner FO (2012) SINA: accurate high-throughput multiple sequence alignment of ribosomal RNA genes. Bioinformatics 28:1823–1829

    Article  CAS  Google Scholar 

  • Reckhardt A et al (2015) Carbon, nutrient and trace metal cycling in sandy sediments: a comparison of high-energy beaches and backbarrier tidal flats. Estuar Coast Shelf Sci 159:1–14

    Article  CAS  Google Scholar 

  • Reisky L et al (2019) A marine bacterial enzymatic cascade degrades the algal polysaccharide ulvan. Nat Chem Biol 15:803–812

    Article  CAS  Google Scholar 

  • Rendueles O, Ghigo J-M (2015) Mechanisms of competition in biofilm communities. In: Microbial biofilms. Wiley, pp 319–342

  • Rice P, Longden I, Bleasby A (2000) EMBOSS: the European molecular biology open software suite. Trends Genet 16:276–277. https://doi.org/10.1016/S0168-9525(00)02024-2

    Article  CAS  Google Scholar 

  • Sack EL, van der Wielen PW, van der Kooij D (2011) Flavobacterium johnsoniae as a model organism for characterizing biopolymer utilization in oligotrophic freshwater environments. Appl Environ Microbiol 77:6931–6938

    Article  CAS  Google Scholar 

  • Scheuerl T, Hopkins M, Nowell RW, Rivett DW, Barraclough TG, Bell T (2020) Bacterial adaptation is constrained in complex communities. Nat Commun 11:1–8

    Article  Google Scholar 

  • Seemann T (2014) Prokka: rapid prokaryotic genome annotation. Bioinformatics 30:2068–2069. https://doi.org/10.1093/bioinformatics/btu153

    Article  CAS  Google Scholar 

  • Stackebrandt E (2006) Taxonomic parameters revisited: tarnished gold standards. Microbiol Today 33:152–155

    Google Scholar 

  • Starliper CE (2011) Bacterial coldwater disease of fishes caused by Flavobacterium psychrophilum. J Adv Res 2:97–108

    Article  Google Scholar 

  • Team RC (2013) R: A language and environment for statistical computing. Vienna, Austria

  • Weisburg WG, Barns SM, Pelletier DA, Lane DJ (1991) 16S ribosomal DNA amplification for phylogenetic study. J Bacteriol 173(2):697–703. https://doi.org/10.1128/jb.173.2.697-703.1991

  • Weon H-Y et al (2007) Flavobacterium terrae sp. nov. and Flavobacterium cucumis sp. nov., isolated from greenhouse soil. Int J Syst Evol Microbiol 57:1594–1598

    Article  Google Scholar 

  • Wickham H (2016) Data analysis. In: ggplot2. Springer, Cham, pp 189–201

  • Yoon J-H, Kang S-J, Lee S-Y (2012) Salinimonas lutimaris sp. nov., a polysaccharide-degrading bacterium isolated from a tidal flat. Antonie Van Leeuwenhoek 101:803–810

    Article  CAS  Google Scholar 

  • Yoon S-H et al (2017) Introducing EzBioCloud: a taxonomically united database of 16S rRNA gene sequences and whole-genome assemblies. Int J Syst Evol Microbiol 67:1613

    Article  CAS  Google Scholar 

  • Zhang H et al (2018) dbCAN2: a meta server for automated carbohydrate-active enzyme annotation. Nucleic Acids Res 46:W95–W101

    Article  CAS  Google Scholar 

  • Zhang H, Xie J, Sun Y, Zheng A, Hu X (2020) A novel green approach for fabricating visible, light sensitive nano-broccoli-like antimony trisulfide by marine Sb (v)-reducing bacteria: Revealing potential self-purification in coastal zones. Enzyme Microb Technol 136:109514

    Article  CAS  Google Scholar 

  • Zhou J et al (2010) A new α-galactosidase from symbiotic Flavobacterium sp. TN17 reveals four residues essential for α-galactosidase activity of gastrointestinal bacteria. Appl Microbiol Biotechnol 88:1297–1309

    Article  CAS  Google Scholar 

Download references

Acknowledgements

The authors acknowledge the National Institute of Biological Resources for kindly supporting the project.

Funding

This work was supported by the National Institute of Biological Resources funded by the Ministry of Environment (No. NIBR202134204).

Author information

Authors and Affiliations

Authors

Contributions

JK designed the study, performed formal analysis, and interpreted the results. JK and DS drafted the manuscript. I-TC, K-EL, and YKS provided resources. JY and DS supervised the study. All authors reviewed the results and approved the final version of the manuscript.

Corresponding authors

Correspondence to Jaewoong Yu or Donghyeok Seol.

Ethics declarations

Conflict of interest

The authors declare that the research described herein was conducted in the absence of any commercial or financial relationships that could be construed as potential conflicts of interest.

Additional information

Communicated by Erko Stackebrandt.

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.

Supplementary file1 (DOCX 700 KB)

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.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kim, J., Cha, IT., Lee, KE. et al. Characteristics and adaptability of Flavobacterium panici BSSL-CR3 in tidal flat revealed by comparative genomic and enzymatic analysis. Arch Microbiol 205, 22 (2023). https://doi.org/10.1007/s00203-022-03359-x

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00203-022-03359-x

Keywords

Navigation