Skip to main content
SpringerLink
Log in

A diverse community of jute (Corchorus spp.) endophytes reveals mutualistic host–microbe interactions

  • Original Article
  • Published:
Annals of Microbiology Aims and scope Submit manuscript

Abstract

Endophytes are plant-associated microbes that live within plants as an integral part of the host metabolism and function. This study aimed to identify the molecular and physiological characteristics of both culturable and non-culturable endophytic bacteria and fungi present in different parts of the jute (Corchorus olitorius) plant. Using universal primers used to amplify hypervariable bacterial 16S rDNA and fungal internal transcribed spacer (ITS) regions of 18S rDNA, we identified five different culturable and 20 non-culturable endophytic bacteria as well as 14 different fungal endophytes from various parts of jute. Biochemical and physiological tests suggest that these microbes may bring a wide range of benefits to their hosts. For example, all five culturable endophytic bacteria were positive for auxin and catalase activity, which may lead to improved root elongation and stress resistance, respectively. These bacteria also have metal uptake, haemolytic and hydrolytic activities that could be useful in medical, environmental and industrial applications. The fungal endophytes were positive for lignin peroxidase, cellulase and xylanase activities, all of which may influence jute physiology. Another important finding was the antifungal activity of one of the fungi against a devastating pernicious fungus that affects hundreds of plant species.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

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

Similar content being viewed by others

References

  • Abouzied MM, Reddy CA (1986) Direct fermentation of potato starch to ethanol by cocultures of Aspergillus niger and Saccharomyces cerevisiae. Appl Environ Microbiol 52(5):1055–1059

    CAS  PubMed Central  PubMed  Google Scholar 

  • Ahmed S, Shafiuddin M, Azam MS, Islam MS, Ghosh A, Khan H (2011) Identification and characterization of jute LTR retrotransposons. Mob Genet Elements 1(1):18–28

    Article  PubMed Central  PubMed  Google Scholar 

  • Ali MM (1958) Aerobic bacteria involved in the retting of jute. Appl Microbiol 6(2):87–89

    CAS  PubMed Central  PubMed  Google Scholar 

  • Anderson IC, Cairney JW (2004) Diversity and ecology of soil fungal communities: increased understanding through the application of molecular techniques. Environ Microbiol 6(8):769–779

    Article  CAS  PubMed  Google Scholar 

  • Araújo WL, Maccheroni W Jr, Aguilar-Vildoso CI, Barroso PA, Saridakis HO, AzeVedo JL (2001) Variability and interactions between endophytic bacteria and fungi isolated from leaf tissues of citrus rootstocks. Can J Microbiol 47(3):229–236

    Article  PubMed  Google Scholar 

  • Azevedo JL, Maccheroni W Jr, Pereira JO, de Araújo WL (2000) Endophytic microorganisms: a review on insect control and recent advances on tropical plants. Electron J Biotechnol 3(1):40–65

    Article  Google Scholar 

  • Barros IA, Araújo WL, Azevedo JL (2010) The effect of different growth regimes on the endophytic bacterial communities of the fern, Dicksonia sellowiana hook (Dicksoniaceae). Braz J Microbiol 41(4):956–965

  • Bateman D, Basham H (1976) Degradation of plant cell walls and membranes by microbial enzymes. Physiol Plant Pathol 4:316–355

  • Boddey RM, Urquiaga S, Alves BJ, Reis V (2003) Endophytic nitrogen fixation in sugarcane: present knowledge and future applications. Plant Soil 252(1):139–149

    Article  CAS  Google Scholar 

  • Bodenhausen N, Bortfeld-Miller M, Ackermann M, Vorholt JA (2014) A synthetic community approach reveals plant genotypes affecting the phyllosphere microbiota. PLoS Genet 10(4):e1004283

    Article  PubMed Central  PubMed  Google Scholar 

  • Boer Sd, Copeman R (1974) Endophytic bacterial flora in Solanum tuberosum and its significance in bacterial ring rot diagnosis. Can J Plant Sci 54(1):115–122

    Article  Google Scholar 

  • Brooks DS, Gonzalez CF, Appel DN, Filer T (1994) Evaluation of endophytic bacteria as potential biological-control agents for Oak Wilt. Biol Control 4(4):373–381

    Article  Google Scholar 

  • Bulder C (1955) Some observations on the lipolytic activity of micro-organisms and a new method for its detection. Antonie Van Leeuwenhoek 21(1):433–445

    Article  CAS  PubMed  Google Scholar 

  • Burd GI, Dixon DG, Glick BR (2000) Plant growth-promoting bacteria that decrease heavy metal toxicity in plants. Can J Microbiol 46(3):237–245

    Article  CAS  PubMed  Google Scholar 

  • Carole TM, Pellegrino J, Paster MD (2004) Opportunities in the industrial biobased products industry. Proceedings of the Twenty-Fifth Symposium on Biotechnology for Fuels and Chemicals Held May 4–7, 2003, in Breckenridge, CO, Springer

  • Carrim AJI, Barbosa EC, Vieira JDG (2006) Enzymatic activity of endophytic bacterial isolates of Jacaranda decurrens. Braz Arch Biol Technol 49(3):353–359

    Article  Google Scholar 

  • Cihangir N, Sarikaya E (2004) Investigation of lipase production by a new isolate of Aspergillus sp. World J Microbiol Biotechnol 20(2):193–197

    Article  CAS  Google Scholar 

  • Dalling JW, Davis AS, Schutte BJ, Elizabeth Arnold A (2011) Seed survival in soil: interacting effects of predation, dormancy and the soil microbial community. J Ecol 99(1):89–95

    Article  Google Scholar 

  • Debjit KM, Anilava K (2008) Ecotoxicological effects of jute retting on the survival of two freshwater fish and two invertebrates. Ecotoxicology 17(3):207–211

    Article  Google Scholar 

  • Douady CJ, Delsuc F, Boucher Y, Doolittle WF, Douzery EJ (2003) Comparison of Bayesian and maximum likelihood bootstrap measures of phylogenetic reliability. Mol Biol Evol 20(2):248–254

    Article  CAS  PubMed  Google Scholar 

  • Faruque SM, Naser IB, Islam MJ, Faruque ASG, Ghosh AN, Nair GB, Sack DA, Mekalanos JJ (2004) Seasonal epidemics of cholera inversely correlate with the prevalence of environmental cholera phages. Proc Natl Acad Sci USA 102(5):1702–1707

    Article  Google Scholar 

  • Ferreira A, Quecine MC, Lacava PT, Oda S, Azevedo JL (2008) Diversity of endophytic bacteria from Eucalyptus species seeds and colonization of seedlings by Pantoea agglomerans. FEMS Microbiol Lett 287(1):8–14

  • Fisher P, Petrini O, Scott HL (1992) The distribution of some fungal and bacterial endophytes in maize (Zea mays L.). New Phytol 122(2):299–305

    Article  Google Scholar 

  • Fujii K, Sugimura T, Nakatake K (2010) Ascomycetes with cellulolytic, amylolytic, pectinolytic, and mannanolytic activities inhabiting dead beech (Fagus crenata) trees. Folia Microbiol 55(1):29–34

    Article  CAS  Google Scholar 

  • Garbeva P, Van Overbeek L, Van Vuurde J, Van Elsas J (2001) Analysis of endophytic bacterial communities of potato by plating and denaturing gradient gel electrophoresis (DGGE) of 16S rDNA based PCR fragments. Microb Ecol 41(4):369–383

    Article  CAS  PubMed  Google Scholar 

  • Germida JJ, Siciliano SD, Renato de Freitas J, Seib AM (1998) Diversity of root‐associated bacteria associated with field‐grown canola (Brassica napus L.) and wheat (Triticum aestivum L.). FEMS Microbiol Ecol 26(1):43–50

    Article  CAS  Google Scholar 

  • Goveas SW, Madtha R, Nivas SK, D’Souza L (2011) Isolation of endophytic fungi from Coscinium fenestratum-a red listed endangered medicinal plant. Eurasia J Biosci 5:48–53

    Article  Google Scholar 

  • Green MR, Sambrook J (2012) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory, New York

    Google Scholar 

  • Hallmann J (2001) Plant interactions with endophytic bacteria. In: Jeger MJ, Spence NJ (eds) Biotic interactions in plant–pathogen associations. CABI, Wallingford, pp 87–119

  • Hankin L, Anagnostakis S (1975) The use of solid media for detection of enzyme production by fungi. Mycologia: 597–607

  • Hardoim PR, van Overbeek LS, Elsas JDV (2008) Properties of bacterial endophytes and their proposed role in plant growth. Trends Microbiol 16(10):463–471

    Article  CAS  PubMed  Google Scholar 

  • Hasnain S, Sabri AN (1997) Growth stimulation of Triticum aestivum seedlings under Cr-stresses by non-rhizospheric pseudomonad strains. Environ Pollut 97(3):265–273

    Article  CAS  PubMed  Google Scholar 

  • Hung PQ, Annapurna K (2004) Isolation and characterization of endophytic bacteria in soybean (Glycine sp.). Omonrice 12:92–101

    Google Scholar 

  • Islam MS, Haque MS, Islam MM, Emdad EM, Halim A, Hossen QM, Hossain MZ, Ahmed B, Rahim S, Rahman MS, Alam MM, Hou S, Wan X, Saito JA, Alam M (2012) Tools to kill: genome of one of the most destructive plant pathogenic fungi Macrophomina phaseolina. BMC Genomics 13(1):493

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Jha P, Kumar A (2007) Endophytic colonization of Typha australis by a plant growth‐promoting bacterium Klebsiella oxytoca strain GR‐3. J Appl Microbiol 103(4):1311–1320

    Article  CAS  PubMed  Google Scholar 

  • Khan Z, Doty SL (2009) Characterization of bacterial endophytes of sweet potato plants. Plant Soil 322(1–2):197–207

    Article  CAS  Google Scholar 

  • Kilcawley K, Wilkinson M, Fox P (2002) Determination of key enzyme activities in commercial peptidase and lipase preparations from microbial or animal sources. Enzym Microb Technol 31(3):310–320

    Article  CAS  Google Scholar 

  • Kirk TK, Farrell RL (1987) Enzymatic" combustion": the microbial degradation of lignin. Annu Rev Microbiol 41(1):465–501

    Article  CAS  PubMed  Google Scholar 

  • Kobayashi DY, Palumbo JD (2000) Bacterial endophytes and their effects on plants and uses in agriculture. In: Bacon CW, White JF (eds) Microbial endophytes. Marcel Dekker, New York, pp 199–236

  • Kour A, Shawl AS, Rehman S, Sultan P, Qazi PH, Suden P, Khajuria RK, Verma V (2008) Isolation and identification of an endophytic strain of Fusarium oxysporum producing podophyllotoxin from Juniperus recurva. World J Microbiol Biotechnol 24(7):1115–1121

    Article  CAS  Google Scholar 

  • Krishnan P, Bhat R, Kush A, Ravikumar P (2012) Isolation and functional characterization of bacterial endophytes from Carica papaya fruits. J Appl Microbiol 113(2):308–317

    Article  CAS  PubMed  Google Scholar 

  • Kuklinsky‐Sobral J, Araújo WL, Mendes R, Geraldi IO, Pizzirani‐Kleiner AA (2004) Isolation and characterization of soybean‐associated bacteria and their potential for plant growth promotion. Environ Microbiol 6(12):1244–1251

    Article  PubMed  Google Scholar 

  • Li H-Y, Li D-W, He C-M, Zhou Z-P, Mei T, Xu H-M (2012) Diversity and heavy metal tolerance of endophytic fungi from six dominant plant species in a Pb–Zn mine wasteland in China. Fungal Ecol 5(3):309–315

    Article  Google Scholar 

  • Long HH, Furuya N, Kurose D, Takeshita M, Takanami Y (2003) Isolation of endophytic bacteria from Solanum sp. and their antibacterical activity against plant pathogenic bacteria. Agris 48(1):21–28

  • Long HH, Schmidt DD, Baldwin IT (2008) Native bacterial endophytes promote host growth in a species-specific manner; phytohormone manipulations do not result in common growth responses. PLoS ONE 3(7):e2702

    Article  PubMed Central  PubMed  Google Scholar 

  • Lowe SE, Theodorou M, Trinci A (1987) Cellulases and xylanase of an anaerobic rumen fungus grown on wheat straw, wheat straw holocellulose, cellulose, and xylan. Appl Environ Microbiol 53(6):1216–1223

    CAS  PubMed Central  PubMed  Google Scholar 

  • Ma Y, Rajkumar M, Luo Y, Freitas H (2011) Inoculation of endophytic bacteria on host and non-host plants—effects on plant growth and Ni uptake. J Hazard Mater 195:230–237

    Article  CAS  PubMed  Google Scholar 

  • Mack KM, Rudgers JA (2008) Balancing multiple mutualists: asymmetric interactions among plants, arbuscular mycorrhizal fungi, and fungal endophytes. Oikos 117(2):310–320

    Article  Google Scholar 

  • Madhaiyan M, Poonguzhali S, Senthilkumar M, Seshadri S, Chung H (2004) Growth promotion and induction of systemic resistance in rice cultivar Co-47 (Oryza sativa L.) by Methylobacterium spp. Bot Bull Acad Sinica 45

  • Malinowski DP, Alloush GA, Belesky DP (2000) Leaf endophyte Neotyphodium coenophialum modifies mineral uptake in tall fescue. Plant Soil 227(1–2):115–126

    Article  CAS  Google Scholar 

  • Malinowski DP, Belesky DP (2000) Adaptations of endophyte-infected cool-season grasses to environmental stresses: mechanisms of drought and mineral stress tolerance. Crop Sci 40(4):923–940

    Article  CAS  Google Scholar 

  • Martin KJ, Rygiewicz PT (2005) Fungal-specific PCR primers developed for analysis of the ITS region of environmental DNA extracts. BMC Microbiol 5(1):28

    Article  PubMed Central  PubMed  Google Scholar 

  • McKendrick S, Leake J, Taylor D, Read D (2000) Symbiotic germination and development of myco‐heterotrophic plants in nature: ontogeny of Corallorhiza trifida and characterization of its mycorrhizal fungi. New Phytol 145(3):523–537

    Article  Google Scholar 

  • Miller GL, Blum R, Glennon WE, Burton AL (1960) Measurement of carboxymethylcellulase activity. Anal Biochem 1(2):127–132

    Article  CAS  Google Scholar 

  • Misaghi I, Donndelinger C (1990) Endophytic bacteria in symptom-free cotton plants. Phytopathology 80(9):808–811

    Article  Google Scholar 

  • Mosca CO, Moragues MD, Llovo J, Al Mosaid A, Coleman DC, Ponton J (2003) Casein agar: a useful medium for differentiating Candida dubliniensis from Candida albicans. J Clin Microbiol 41(3):1259–1262

  • Mundt JO, Hinkle NF (1976) Bacteria within ovules and seeds. Appl Environ Microbiol 32(5):694–698

    CAS  PubMed Central  PubMed  Google Scholar 

  • Munshi TK, Chattoo BB (2008) Bacterial population structure of the jute-retting environment. Microb Ecol 56(2):270–282

    Article  PubMed  Google Scholar 

  • Nagata S, Yamaji K, Nomura N, Ishimoto H (2014) Root endophytes enhance stress‐tolerance of Cicuta virosa L. growing in a mining pond of eastern Japan. Plant Species Biol. doi:10.1111/1442-1984.12039

    Google Scholar 

  • Okunishi S, Sako K, Mano H, Imamura A, Morisaki H (2005) Bacterial flora of endophytes in the maturing seed of cultivated rice (Oryza sativa) microbes and environments. Microbes Environ 20(3):168–177

    Article  Google Scholar 

  • Oses R, Valenzuela S, Freer J, Sanfuentes E, Rodriguez J (2008) Fungal endophytes in xylem of healthy Chilean trees and their possible role in early wood decay. Fungal Divers 33:77–86

    Google Scholar 

  • Polidoros A, Mylona P, Scandalios J (2001) Transgenic tobacco plants expressing the maize Cat2 gene have altered catalase levels that affect plant-pathogen interactions and resistance to oxidative stress. Transgenic Res 10(6):555–569

    Article  CAS  PubMed  Google Scholar 

  • Quadt-Hallmann A, Hallmann J, Kloepper J (1997) Bacterial endophytes in cotton: location and interaction with other plant-associated bacteria. Can J Microbiol 43(3):254–259

    Article  CAS  Google Scholar 

  • Rosenblueth M, Martínez-Romero E (2006) Bacterial endophytes and their interactions with hosts. Mol Plant Microbe Interact 19(8):827–837

    Article  CAS  PubMed  Google Scholar 

  • Ruiz MV, Silva P, Laciar A (2009) Comparison of microplate, agar drop and well diffusion plate methods for evaluating hemolytic activity of Listeria monocytogenes. Afr J Microbiol Res 3(6):319–324

    Google Scholar 

  • Rungjindamai N, Pinruan U, Choeyklin R, Hattori T, Jones E (2008) Molecular characterization of basidiomycetous endophytes isolated from leaves, rachis and petioles of the oil palm, Elaeis guineensis. Fungal Divers 33:139–161

    Google Scholar 

  • Sandhya C, Sumantha A, Szakacs G, Pandey A (2005) Comparative evaluation of neutral protease production by Aspergillus oryzae in submerged and solid-state fermentation. Process Biochem 40(8):2689–2694

    Article  CAS  Google Scholar 

  • Saxena M, Kumar A, Chaudhari P, Shivachandra S, Singh V, Sharma B (2005) Ribotyping of Indian isolates of Pasteurella multocida based on 16S and 23S rRNA genes. Vet Res Commun 29(6):527–535

    Article  CAS  PubMed  Google Scholar 

  • Sinsabaugh RL, Carreiro MM, Alvarez S (2002) Enzyme and microbial dynamics of litter decomposition. In: Burns RG, DickRP (eds) Enzymes in the environment, activity, ecology, and applications. Marcel Dekker, New York, pp 249–265

  • Strobel G, Daisy B, Castillo U, Harper J (2004) Natural products from endophytic microorganisms. J Nat Prod 67(2):257–268

    Article  CAS  PubMed  Google Scholar 

  • Sturz A, Christie B, Matheson B, Nowak J (1997) Biodiversity of endophytic bacteria which colonize red clover nodules, roots, stems and foliage and their influence on host growth. Biol Fertil Soils 25(1):13–19

    Article  Google Scholar 

  • Tamas L, Dudikova J, Durcekova K, Haluskova L, Huttova J, Mistrik I, Olle M (2008) Alterations of the gene expression, lipid peroxidation, proline and thiol content along the barley root exposed to cadmium. J Plant Physiol 165(11):1193–1203

    Article  CAS  PubMed  Google Scholar 

  • Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. J Mol Evol 30(12):2725–2729

    Article  CAS  Google Scholar 

  • Teather RM, Wood PJ (1982) Use of Congo red-polysaccharide interactions in enumeration and characterization of cellulolytic bacteria from the bovine rumen. Appl Environ Microbiol 43(4):777–780

    CAS  PubMed Central  PubMed  Google Scholar 

  • Thomas P, Swarna GK, Roy PK, Patil P (2008) Identification of culturable and originally non-culturable endophytic bacteria isolated from shoot tip cultures of banana cv grand naine. Plant Cell Tissue Organ Cult 93(1):55–63

    Article  Google Scholar 

  • Tyler HL, Triplett EW (2008) Plants as a habitat for beneficial and/or human pathogenic bacteria. Annu Rev Phytopathol 46:53–73

    Article  CAS  PubMed  Google Scholar 

  • Verma SC, Ladha JK, Tripathi AK (2001) Evaluation of plant growth promoting and colonization ability of endophytic diazotrophs from deep water rice. J Biotechnol 91(2):127–141

    Article  CAS  PubMed  Google Scholar 

  • Zarcinas B, Cartwright B, Spouncer L (1987) Nitric acid digestion and multi‐element analysis of plant material by inductively coupled plasma spectrometry. Commun Soil Sci Plant Anal 18(1):131–146

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We would like to acknowledge the contributions and support of Mahdi Mohammad Moosa, Arif Mohammad Tanmoy, Tariqul Islam, Ahlan Sabah Ferdous, Samira Busra, Kamal Hossain of the Molecular Biology Laboratory, University of Dhaka and Md. Shahidul Islam of the Bangladesh Jute Research Institute. Farhana Shafrin is the recipient of a Ph.D. fellowship from the Bangladesh Academy of Sciences.

Conflicts of interest

The authors declare that there are no conflicts of interest regarding the publication of this paper.

Author information

Authors and Affiliations

  1. Molecular Biology Laboratory, Department of Biochemistry and Molecular Biology, University of Dhaka, Dhaka, Bangladesh

    Rifat Ara Najnin, Farhana Shafrin, Ahsan Habib Polash, Aubhishek Zaman, Amzad Hossain, Taha Taha, Rajib Ahmed, Jannatul Ferdoush Tuli, Rashu Barua & Haseena Khan

  2. Department of Biotechnology and Genetic Engineering, University of Dhaka, Dhaka, Bangladesh

    Farhana Shafrin, Ahsan Habib Polash, Aubhishek Zaman & Abu Ashfaqur Sajib

Authors
  1. Rifat Ara Najnin
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Farhana Shafrin
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ahsan Habib Polash
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Aubhishek Zaman
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Amzad Hossain
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Taha Taha
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Rajib Ahmed
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Jannatul Ferdoush Tuli
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Rashu Barua
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Abu Ashfaqur Sajib
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Haseena Khan
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Haseena Khan.

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

(DOC 8044 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Najnin, R.A., Shafrin, F., Polash, A.H. et al. A diverse community of jute (Corchorus spp.) endophytes reveals mutualistic host–microbe interactions. Ann Microbiol 65, 1615–1626 (2015). https://doi.org/10.1007/s13213-014-1001-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13213-014-1001-1

Keywords

Search

Navigation