Skip to main content

Metagenomic profiling of bacterial diversity and community structure in termite mounds and surrounding soils

Archives of Microbiology volume 202, pages 2697–2709 (2020)Cite this article

Abstract

The study focuses on analysis of the compositional and diversity of bacteria in termite mound soils in comparison with the surrounding soils to verify the assertion that the high nutrient concentrations in termite mound soils influence a complex diversity of microorganisms. Here, whole DNA was extracted from soil samples collected from termite mounds and their surrounding soils which were 10 m apart and subsequently, sequenced using shotgun metagenomic approach. Our findings showed that both environments have several soil bacterial phyla in common. However, Proteobacteria and Actinobacteria significantly dominated the termite mound soils and the surrounding soils, respectively, with Tenericutes peculiar to only the termite mound soils. Furthermore, Bergeyella, Gloeothece, Thalassospira, and Glaciecola genera were exclusively identified in the termite mound soil samples. Diversity analysis showed that bacterial composition was different among the four sites (phyla level). This study also revealed a lot of unclassified groups of bacteria and this could point to the presence of potentially novel species. The differences observed in the bacterial structure and diversity from this study may be ascribed to variances in the physicochemical nature existing between the two environments. Mapping out schemes to culture these unclassified groups of bacteria discovered from this study would possibly set the platform for the discovery of novel bacteria for biotechnological applications.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

43,34 €

Price includes VAT (Finland)
Tax calculation will be finalised during checkout.

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

Data availability

The quality sequences are available from NCBI SRA dataset under the bioproject PRJNA526912 for termite mound soil samples and PRJNA525146 for the surrounding soil samples.

References

  • Ali IG, Sheridan G, French J (2013) Ecological benefits of termite soil interaction and microbial symbiosis in the soil ecosystem. J Earth Sci Geotech Engr 3:63–85

    CAS  Google Scholar 

  • Arif A, Muin M, Larekeng S, Lestari P (2019) Survey and morphological identification of termites (Insecta: Isoptera) in teaching forest of Hasanuddin University Indonesia. IOP Conf Ser Earth Environ Sci 270:012001

    Google Scholar 

  • Arumugam M, Pushpanathan M, Sathyavathi S, Gunasekaran P, Rajendhran J (2016) Comparative analysis of microbial diversity in termite gut and termite nest using ion sequencing. Curr Microbiol 72:267–275

    Google Scholar 

  • Bignell DE, Roisin Y, Lo N (eds) (2011) Biology of termites: a modern synthesis. Springer, Netherlands

    Google Scholar 

  • Brauman A, Bignell DE, Tayasu I (2000) Soil-feeding termites: biology, microbial associations and digestive mechanisms. Termites: evolution, sociality, symbioses, ecology. Springer, Dordrecht, pp 233–259

    Google Scholar 

  • Castañeda LE, Barbosa O (2017) Metagenomic analysis exploring taxonomic and functional diversity of soil microbial communities in Chilean vineyards and surrounding native forests. PeerJ 5:e3098

    PubMed  PubMed Central  Google Scholar 

  • Chauhan AK, Maheshwari DK, Dheeman S, Bajpai VK (2017) Termitarium-inhabiting Bacillus spp. enhanced plant growth and bioactive component in turmeric (Curcuma longa L.). Curr Microbiol 74:184–192

    CAS  PubMed  Google Scholar 

  • Cheik S, Bottinelli N, Soudan B, Harit A, Chaudhary E, Sukumar R, Jouquet P (2019) Effects of termite foraging activity on topsoil physical properties and water infiltration in Vertisol. Appl Soil Ecol 133:132–137

    Google Scholar 

  • Chouvenc T, Su N-Y, Robert A (2010) Inhibition of the fungal pathogen Metarhizium anisopliae in the alimentary tracts of five termite (Isoptera) species. Florida Ento 93:467–469

    Google Scholar 

  • Clarke K, Green R (1988) Statistical design and analysis for a" biological effects" study. Marine Ecol Progress Series 46:213–226

    Google Scholar 

  • Deke AL, Adugna WT, Fite AT (2016) Soil physic-chemical properties in termite mounds and adjacent control soil in Miyo and Yabello Districts of Borana Zone, Southern Ethiopia. Am J Agric Forestry 4:69–74

    Google Scholar 

  • Dhembare A (2013) Physico-chemical properties of termite mound soil. Arch Appl Sci Res 5:123–126

    Google Scholar 

  • Duponnois R, Paugy M, Thioulouse J, Masse D, Lepage M (2005) Functional diversity of soil microbial community, rock phosphate dissolution and growth of Acacia seyal as influenced by grass-, litter- and soil-feeding termite nest structure amendments. Geoderma 124:349–361

    CAS  Google Scholar 

  • Enagbonma BJ, Babalola OO (2019a) Environmental sustainability: a review of termite mound soil material and its bacteria. Sustainability 11:3847

    CAS  Google Scholar 

  • Enagbonma BJ, Babalola OO (2019b) Potentials of termite mound soil bacteria in ecosystem engineering for sustainable agriculture. Ann Microbiol 69:211–219

    Google Scholar 

  • Enagbonma BJ, Babalola OO (2020) Unveiling plant-beneficial function as seen in bacteria genes from termite mound soil. J Soil Sci Plant Nutr 20:421–430

    CAS  Google Scholar 

  • Fall S, Nazaret S, Chotte J, Brauman A (2004) Bacterial density and community structure associated with aggregate size fractions of soil-feeding termite mounds. Microbial Ecol 48(2):191–199

    CAS  Google Scholar 

  • Fall S, Hamelin J, Ndiaye F, Assigbetse K, Aragno M, Chotte JL, Brauman A (2007) Differences between bacterial communities in the gut of a soil-feeding termite (Cubitermes niokoloensis) and its mounds. Appl Environ Microbiol 73:5199–5208

    CAS  PubMed  PubMed Central  Google Scholar 

  • Faoro H et al (2010) Influence of soil characteristics on the diversity of bacteria in the Southern Brazilian Atlantic Forest. Appl Environ Microbiol 76:4744–4749

    CAS  PubMed  PubMed Central  Google Scholar 

  • Fierer N et al (2012) Cross-biome metagenomic analyses of soil microbial communities and their functional attributes. Proc Nat Acad Sci 109:21390–21395

    CAS  PubMed  Google Scholar 

  • Green B, Bardunias P, Turner JS, Nagpal R, Werfel J (2017) Excavation and aggregation as organizing factors in de novo construction by mound-building termites. Proc Bio Sci 284:20162730

    Google Scholar 

  • Hammer Ř, Harper D, Ryan P (2001) PAST: Paleontological statistics software package for education and data analysis–palaeontol. Electron 4:9–15

    Google Scholar 

  • Harry M, Jusseaume N, Gambier B, Garnier-Sillam E (2001) Use of RAPD markers for the study of microbial community similarity from termite mounds and tropical soils. Soil Bio Biochem 33:417–427

    CAS  Google Scholar 

  • Hayat R, Ali S, Amara U, Khalid R, Ahmed I (2010) Soil beneficial bacteria and their role in plant growth promotion: a review. Ann Microbiol 60:579–598

    Google Scholar 

  • Ibarbalz FM, Pérez MV, Figuerola EL, Erijman L (2014) The bias associated with amplicon sequencing does not affect the quantitative assessment of bacterial community dynamics. PLoS ONE 9:e99722

    PubMed  PubMed Central  Google Scholar 

  • Kent WJ (2002) BLAT—the BLAST-like alignment tool. Genome Res 12:656–664

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kettler T, Doran JW, Gilbert T (2001) Simplified method for soil particle-size determination to accompany soil-quality analyses. Soil Sci Soc Am J 65:849–852

    CAS  Google Scholar 

  • Khomtchouk BB, Hennessy JR, Wahlestedt C (2017) Shinyheatmap: ultra fast low memory heatmap web interface for big data genomics. PLoS ONE 12:e0176334

    PubMed  PubMed Central  Google Scholar 

  • Lan Y, Rosen G, Hershberg R (2016) Marker genes that are less conserved in their sequences are useful for predicting genome-wide similarity levels between closely related prokaryotic strains. Microbiome 4:18

    PubMed  PubMed Central  Google Scholar 

  • Lima SSD, Pereira MG, Santos GLD, Pontes RdM, Diniz AR (2018) Soil physical and chemical properties in epigeal termite mounds in pastures. Floresta e Ambiente 25:e20160110

    Google Scholar 

  • Liu X, Pan J, Liu Y, Li M, Gu J (2018) Diversity and distribution of archaea in global estuarine ecosystems. Sci Total Environ 637–638:349–358

    PubMed  Google Scholar 

  • Makonde HM, Mwirichia R, Osiemo Z, Boga HI, Klenk HP (2015) 454 Pyrosequencing-based assessment of bacterial diversity and community structure in termite guts, mounds and surrounding soils. SpringerPlus 4:471

    PubMed  PubMed Central  Google Scholar 

  • Manjula A, Sathyavathi S, Pushpanathan M, Gunasekaran P, Rajendhran J (2014) Microbial diversity in termite nest. Curr Sci 106:1430–1434

    Google Scholar 

  • McBratney A, Field DJ, Koch A (2014) The dimensions of soil security. Geoderma 213:203–213

    Google Scholar 

  • Meyer F et al (2008) The metagenomics RAST server–a public resource for the automatic phylogenetic and functional analysis of metagenomes. BMC Bioinf 9:386

    CAS  Google Scholar 

  • Miyagawa S et al (2011) Indigenous utilization of termite mounds and their sustainability in a rice growing village of the Central Plain of Laos. J Ethnobio Ethnomed 7:24

    Google Scholar 

  • Muwawa EM, Makonde HM, Budambula N, Osiemo ZL (2010) Chemical properties associated with guts, soil and nest materials of Odontotermes and Macrotermes species from Kenya. J Bio Environ Sci 4:253–263

    Google Scholar 

  • Nithyatharani R, Kavitha U (2018) Termite soil as bio-indicator of soil fertility. Int J Res Appl Sci Eng Tech 6:659–661

    Google Scholar 

  • Ntambo R, Boga H, Muigai A, Mwirichia R (2010) Isolation and characterization of bacteria isolates from soil feeding termites and soil from Juja and Kakamega forest in Kenya. In: JKUAT Scientific Technological and Industrialization Conference, Jomo Kanyatta University of Agriculture and Technology 2010. Digetal Repository

  • Paul J, Varma A (1993) Characterization of cellulose and hemicellulose degrading Bacillus sp. from termite infested soil. Curr Sci 64:262–266

    CAS  Google Scholar 

  • Probst AJ, Moissl-Eichinger C (2015) "Altiarchaeales": uncultivated archaea from the subsurface. Life 5(2):1381–1395

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ranjan R, Rani A, Metwally A, McGee HS, Perkins DL (2016) Analysis of the microbiome: advantages of whole genome shotgun versus 16S amplicon sequencing. Biochem Biophys Res Commun 469:967–977

    CAS  PubMed  PubMed Central  Google Scholar 

  • Rückamp D, Martius C, Bornemann L, Kurzatkowski D, Naval LP, Amelung W (2012) Soil genesis and heterogeneity of phosphorus forms and carbon below mounds inhabited by primary and secondary termites. Geoderma 170:239–250

    Google Scholar 

  • Shi J-Y, Yuan X-F, Lin H-R, Yang Y-Q, Li Z-Y (2011) Differences in soil properties and bacterial communities between the rhizosphere and bulk soil and among different production areas of the medicinal plant Fritillaria thunbergii. Int J Mol Sci 12:3770–3785

    CAS  PubMed  PubMed Central  Google Scholar 

  • Spain AM, Krumholz LR, Elshahed MS (2009) Abundance, composition, diversity and novelty of soil Proteobacteria. ISME J 3:992

    CAS  PubMed  Google Scholar 

  • Takematsu Y, Vongkaluang C (2012) A taxonomic review of the Rhinotermitidae (Isoptera) of Thailand. J Nat Hist 46(17–18):1079–1109

    Google Scholar 

  • Walkley A, Black IA (1934) An examination of the Degtjareff method for determining soil organic matter, and a proposed modification of the chromic acid titration method. Soil Sci 37:29–38

    CAS  Google Scholar 

  • Wilke A et al (2012) The M5nr: a novel non-redundant database containing protein sequences and annotations from multiple sources and associated tools. BMC Bioinf 13:141

    CAS  Google Scholar 

  • Wang H et al (2015) Quality of fresh organic matter affects priming of soil organic matter and substrate utilization patterns of microbes. Sci Rep 5:10102

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yun Y et al (2016) The relationship between pH and bacterial communities in a Single Karst ecosystem and its implication for soil acidification. Front Microbiol 7:1955

    PubMed  PubMed Central  Google Scholar 

  • Zhu L-X, Xiao Q, Shen Y-F, Li S-Q (2017) Microbial functional diversity responses to 2 years since biochar application in silt-loam soils on the Loess Plateau Ecotoxicol. Environ Safe 144:578–584

    CAS  Google Scholar 

Download references

Acknowledgments

B.J.E. thanks South Africa’s National Research Foundation/The World Academy of Science African Renaissance Grant (UID110909) for stipend that was of great help during his Doctoral programme. O.O.B. would like to thank the National Research Foundation, South Africa for the Grant (UID123634) that has supported research in her lab.

Funding

This research was funded by South Africa’s National Research Foundation (UID123634).

Author information

Affiliations

  1. Food Security and Safety Niche, Faculty of Natural and Agricultural Sciences, North-West University, Private Mail Bag X2046, Mmabatho, 2735, South Africa

    Ben Jesuorsemwen Enagbonma, Caroline Fadeke Ajilogba & Olubukola Oluranti Babalola

Authors
  1. Ben Jesuorsemwen Enagbonma
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Caroline Fadeke Ajilogba
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Olubukola Oluranti Babalola
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

BJE is a PhD candidate, who managed the literature searches, carries out the laboratory work, performed the analyses, interpretation of results and wrote the first draft of the manuscript. CFD proof read the draft and assisted in the analysis using R while OOB is the principal investigator, provided academic input, thoroughly critiqued the manuscript and funded the totality of the research from DNA extraction kits to NGS sequencing. All authors approved the article for publication.

Corresponding author

Correspondence to Olubukola Oluranti Babalola.

Ethics declarations

Conflict of interests:

The authors declare that they have no competing interests.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Communicated by Erko Stackebrandt.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 514 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Enagbonma, B.J., Ajilogba, C.F. & Babalola, O.O. Metagenomic profiling of bacterial diversity and community structure in termite mounds and surrounding soils. Arch Microbiol 202, 2697–2709 (2020). https://doi.org/10.1007/s00203-020-01994-w

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00203-020-01994-w

Keywords

  • Amplicon sequencing
  • Bacterial composition
  • Illumina platforms
  • Termitarium
  • Whole genome