Abstract
Fruit peels, also known as rinds or skins, are wastes readily available in large quantities. Here, we have used pineapple (PA) and watermelon (WM) peels as substrates in the culture media (containing 5 % sucrose and 0.7 % ammonium sulfate) for production of bacterial cellulose (BC). The bacterial culture used in the study, Komagataeibacter hansenii produced BC under static conditions as a pellicle at the air–liquid interface in standard Hestrin and Schramm (HS) medium. The yield obtained was ~3.0 g/100 ml (on a wet weight basis). The cellulosic nature of the pellicle was confirmed by CO2, H2O, N2, and SO2 (CHNS) analysis and Fourier transform infrared (FT-IR) spectroscopy. Scanning electron microscopy (SEM) and atomic force microscopy (AFM) of the pellicle revealed the presence of flat twisted ribbonlike fibrils (70–130 nm wide). X-ray diffraction analysis proved its crystalline nature (matching cellulose I) with a crystallinity index of 67 %. When K. hansenii was grown in PA and WM media, BC yields were threefolds or fourfolds higher than those obtained in HS medium. Interestingly, textural characterization tests (viz., SEM, crystallinity index, resilience, hardness, adhesiveness, cohesiveness, springiness, shear energy and stress, and energy required for puncturing the pellicle) proved that the quality of BC produced in PA and WM media was superior to the BC produced in HS medium. These findings demonstrate the utility of the newly designed media for getting higher yields and better quality of BC, which could make fermentative production of BC more attractive on a commercial scale.




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References
Anon (2012) FSSAI lab manual no. 5. Manual of methods of analysis of foods (fruits and vegetables). Government of India, New Delhi
Ashori A, Sheykhnazari S, Tabarsa T, Shakeri A, Golalipour M (2012) Bacterial cellulose/silica nanocomposites: preparation and characterization. Carbohydr Polym 90:413–418. doi:10.1016/j.carbpol.2012.05.060
Aydin YA, Aksoy ND (2009) Isolation of cellulose producing bacteria from wastes of vinegar fermentation. Proceedings of the World Congress on Engineering and Computer Science I:20–23
Aydin YA, Aksoy ND (2014) Isolation and characterization of an efficient bacterial cellulose producer strain in agitated culture: Gluconacetobacter hansenii P2A. Appl Microbiol Biotechnol 98:1065–1075. doi:10.1007/s00253-013-5296-9
Bae S, Shoda M (2005) Statistical optimization of culture conditions for bacterial cellulose production using Box-Behnken design. Biotechnol Bioeng 90:20–28. doi:10.1002/bit.20325
Barud HS, Ribeiro SJL, Carone CL, Ligabue R, Einloft S, Queiroz PVS, Borges APB, Jahno VD (2013) Optically transparent membrane based on bacterial cellulose/polycaprolactone. Polímeros 23:135–138. doi:10.1590/S0104-14282013005000018
Blaker JJ, Lee KY, Mantalaris A, Bismarck A (2010) Ice-microsphere templating to produce highly porous nanocomposite PLA matrix scaffolds with pores selectively lined by bacterial cellulose nano-whiskers. Compos Sci Technol 70:1879–1888. doi:10.1016/j.compscitech.2010.05.028
Bottom R (2008) Thermogravimetric analysis. In: Gabbott P (ed) Principles and applications of thermal analysis. Blackwell Publishing, UK, pp 87–118
Bridson EY, Brecker A (1970) Chapter III Design and formulation of microbial culture media. In: Norris JR, Ribbons DW (eds) Methods in microbiology. U.S. Academic Press Inc., pp 22–295
Budhiono A, Rosidi B, Taher H, Iguchi M (1999) Kinetic aspects of bacterial cellulose focbrsrmation in nata-de-coco culture system. Carbohydr Polym 40:137–143. doi:10.1016/S0144-8617(99)00050-8
Campbell M (2006) Extraction of pectin from watermelon rind. Dissertation, Oklahoma State University
Castro C, Zuluaga R, Putaux JL, Caro G, Mondragon I, Gañán P (2011) Structural characterization of bacterial cellulose produced by Gluconacetobacter swingsii sp. from Colombian agroindustrial wastes. Carbohydr Polym 84:96–102. doi:10.1016/j.carbpol.2010.10.072
Castro C, Zuluaga R, Álvarez C, Putaux JL, Caro G, Rojas OJ, Mondragon I, Gañán P (2012) Bacterial cellulose produced by a new acid-resistant strain of Gluconacetobacter genus. Carbohydr Polym 89:1033–1037. doi:10.1016/j.carbpol.2012.03.045
Chao Y, Ishida T, Sugano Y, Shoda M (2000) Bacterial cellulose production by Acetobacter xylinum in a 50‐l internal‐loop airlift reactor. Biotechnol Bioeng 68:345–352. doi:10.1002/(SICI)1097-0290(20000505)68:3<345::AID-BIT13>3.0.CO;2-M
Chawla PR, Bajaj IB, Survase SA, Singhal RS (2009) Microbial cellulose: fermentative production and applications. Food Technol Biotechnol 47:107–124
Chen L, Hong F, Yang XX, Han SF (2013) Biotransformation of wheat straw to bacterial cellulose and its mechanism. Bioresour Technol 135:464–468. doi:10.1016/j.biortech.2012.10.029
Ching CH, Muhammad II (2007) Evaluation and optimization of microbial cellulose (nata) production using pineapple waste as substrate. In: National research and innovation competition (NRIC), Penang, Malaysia
Czaja W, Romanovicz D, Brown RM (2004) Structural investigations of microbial cellulose produced in stationary and agitated culture. Cellulose 11:403–411. doi:10.1023/B:CELL.0000046412.11983.61
Czaja WK, Young DJ, Kawecki M, Brown RM (2007) The future prospects of microbial cellulose in biomedical applications. Biomacromolecules 8:1–12. doi:10.1021/bm060620d
Dobre LM, Stoica-Guzun A, Stroescu M, Jipa IM, Dobre T, Ferdeş M, Ciumpiliac Ş (2012) Modelling of sorbic acid diffusion through bacterial cellulose-based antimicrobial films. Chem Pap 66:144–151. doi:10.2478/s11696-011-0086-2
Dubois M, Gilles KA, Hamilton JK, Rebers P, Smith F (1956) Colorimetric method for determination of sugars and related substances. Anal Chem 28:350–356. doi:10.1021/ac60111a017
Eichhorn SJ, Dufresne A, Aranguren M, Marcovich NE, Capadona JR, Rowan SJ, Weder C, Thielemans W, Roman M, Renneckar S, Gindl W, Veigel S, Keckes J, Yano H, Abe K, Nogi M, Nakagaito AN, Mangalam A, Simonsen J, Benight AS, Bismarck A, Berglund LA, Peijs T (2010) Review: current international research into cellulose nanofibres and nanocomposites. J Mater Sci 45:1–33. doi:10.1007/s10853-009-3874-0
El-Saied H, El-Diwany AI, Basta AH, Atwa NA, El-Ghwas DE (2008) Production and characterization of economical bacterial cellulose. Bioresour 3:1196–1217
Embuscado ME, Marks JS, BeMiller JN (1994) Bacterial cellulose: I. Factors affecting the production of cellulose by Acetobacter xylinum. Food Hydrocolloid 8:407–418. doi:10.1016/S0268-005X(09)80084-2
Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791
Ford ENJ, Mendon SK, Thames SF, Rawlins JW (2010) X-ray diffraction of cotton treated with neutralized vegetable oil-based macromolecular crosslinkers. J Eng Fiber Fabr 5:10–20
Gadim TDO, Figueiredo AGPR, Rosero-Navarro NC, Vilela C, Gamelas JAF, Barros-Timmons A, Neto CP, Silvestre AJD, Freire CSR, Figueiredo FML (2014) Nanostructured bacterial cellulose-poly(4-styrene sulfonic acid) composite membranes with high storage modulus and protonic conductivity. ACS Appl Mater Interfaces 6:7864–7875. doi:10.1021/am501191t
George J, Ramana KV, Sabapathy SN, Bawa AS (2005) Physico-mechanical properties of chemically treated bacterial (Acetobacter xylinum) cellulose membrane. World J Microbiol Biotechnol 21:1323–1327. doi:10.1007/s11274-005-3574-0
Haigler CH, White AR, Brown RM, Cooper KAYM (1982) Alteration of in vivo cellulose ribbon assembly by carboxymethylcellulose and other cellulose derivatives. 94:0–5. PMCID:PMC2112193
Haimer E, Wendland M, Schlufter K, Frankenfeld K, Miethe P, Potthast A, Rosenau T, Liebner F (2010) Loading of bacterial cellulose aerogels with bioactive compounds by antisolvent precipitation with supercritical carbon dioxide. Macromol Symp 294:64–74. doi:10.1002/masy.201000008
Hemalatha R, Anbuselvi S (2013) Physicohemical constituents of pineapple pulp and waste. J Chem Pharm Res 5:240–242
Hong F, Qiu K (2008) An alternative carbon source from konjac powder for enhancing production of bacterial cellulose in static cultures by a model strain Acetobacter aceti subsp. xylinus ATCC 23770. Carbohydr Polym 72:545–549. doi:10.1016/j.carbpol.2007.09.015
Hong F, Zhu YX, Yang G, Yang XX (2011) Wheat straw acid hydrolysate as a potential cost‐effective feedstock for production of bacterial cellulose. J Chem Technol Biol 86:675–680. doi:10.1002/jctb.2567
Hu W, Chen S, Liu L, Ding B, Wang H (2011) Formaldehyde sensors based on nanofibrous polyethyleneimine/bacterial cellulose membranes coated quartz crystal microbalance. Sensors Actuators B Chem 157:554–559. doi:10.1016/j.snb.2011.05.021
Hungund BS, Gupta SG (2010) Strain improvement of Gluconacetobacter xylinus NCIM 2526 for bacterial cellulose production. Afr J Biotechnol 9:5170–5172. doi:10.5897/AJB09.1877
Hungund B, Prabhu S, Shetty C, Acharya S, Prabhu V, Gupta SG (2013) Production of bacterial cellulose from Gluconacetobacter persimmonis GH-2 using dual and cheaper carbon sources. J Microb Biochem Technol 5:2. doi:10.4172/1948-5948.1000095
Jagannath A, Manjunatha SS, Ravi N, Raju PS (2011) The effect of different substrates and processing conditions on the textural characteristics of bacterial cellulose (nata) produced by Acetobacter xylinum. J Food Process Eng 34:593–608. doi:10.1111/j.1745-4530.2009.00403.x
Kersters K, Lisdiyanti P, Komagata K, Swings J (2006) The family Acetobacteraceae: the genera Acetobacter, Acidomonas, Asaia, Gluconacetobacter, Gluconobacter, and Kozakia. In: Falkow S, Rosenberg E, Schleifer KH, Stackebrandt E (eds) The Prokaryotes, 3rd edn. Springer, New York, pp 163–200
Keshk SMAS, Sameshima K (2005) Evaluation of different carbon sources for bacterial cellulose production. Afr J Biotechnol 4:478–482
Keshk SMAS, Razek TMA, Sameshima K (2006) Bacterial Cellulose Production from Beet Molasses. Afr J Biotechnol 5:1519–1523
Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120. doi:10.1007/BF01731581
Klemm D, Schumann D, Udhardt U, Marsch S (2001) Bacterial synthesized cellulose synthesized artificial blood vessels for microsurgery. Prog Polym Sci 26:1561–1603. doi:10.1016/S0079-6700(01)00021-1
Kongruang S (2008) Bacterial cellulose production by Acetobacter xylinum strains from agricultural waste products. Appl Biochem Biotechnol 148:245–256. doi:10.1007/s12010-007-8119-6
Kurosumi A, Sasaki C, Yamashita Y, Nakamura Y (2009) Utilization of various fruit juices as carbon source for production of bacterial cellulose by Acetobacter xylinum NBRC 13693. Carbohydr Polym 76:333–335. doi:10.1016/j.carbpol.2008.11.009
Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23:2947–2948. doi:10.1093/bioinformatics/btm404
Larrauri A, Rupe P, Calixto FS (1997) Pineapple shell as a source of dietary fiber with associated polyphenols. J Agric Food Chem 45:4028–4031. doi:10.1021/jf970450j
Lee KY, Buldum G, Mantalaris A, Bismarck A (2014) More than meets the eye in bacterial cellulose: biosynthesis, bioprocessing, and applications in advanced fiber composites. Macromol Biosci 14:10–32. doi:10.1002/mabi.201300298
Lestari P, Elfrida N, Suryani A, Suryadi Y (2014) Study on the production of bacterial cellulose from Acetobacter xylinum using agro-waste. Jordan J Biol Sci 7:75–80
Lu H, Jiang X (2014) Structure and properties of bacterial cellulose produced using a trickling bed reactor. Appl Biochem Biotech 172:3844–3861. doi:10.1007/s12010-014-0795-4
Mohammadkazemi F, Azin M, Ashori A (2015) Production of bacterial cellulose using different carbon sources and culture media. Carbohydr Polym 117:518–523. doi:10.1016/j.carbpol.2014.10.008
Mohanraj R, Deore PS, Paul N (2011) Phylogeny reconstruction of Acetobacter species by RAPD (random amplified polymorphic DNA) markers. Recent Res Sci Technol 3:100–102
Moosavi-Nasab M, Yousefi AR, Askari H, Bakhtiyari M (2010) Fermentative production and characterization of carboxymethyl bacterial cellulose using date syrup. World Acad Sci Eng Technol 68:1467–1471
Munoz AM (1986) Development and application of texture reference scales. J Sens Stud 1:55–83. doi:10.1111/j.1745-459X.1986.tb00159.x
Muyzer G, De Waal EC, Uitterlinden AG (1993) Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA. Appl Environ Microbiol 59:695–700, PMCID:PMC202176
Nakai T, Tonouchi N, Konishi T, Kojima Y, Tsuchida T, Yoshinaga F, Sakai F, Hayashi T (1999) Enhancement of cellulose production by expression of sucrose synthase in Acetobacter xylinum. Proc Natl Acad Sci U S A 96:14–18. doi:10.1073/pnas.96.1.14
Nelson ML, O’Connor RT (1964) Relation of certain infrared bands to cellulose crystallinity and crystal lattice type: Part II. A new infrared ratio for estimation of crystallinity in celluloses I and II. J Appl Polym Sci 8:1325–1341. doi:10.1002/app.1964.070080323
Park JK, Jung JY, Park YH (2003) Cellulose production by Gluconacetobacter hansenii in a medium containing ethanol. Biotechnol Lett 25:2055–2059. doi:10.1023/B:BILE.0000007065.63682.18
Pourramezan GZ, Roayaei AM, Qezelbash QR (2009) Optimization of culture conditions for bacterial cellulose production by Acetobacter sp. 4B-2. Biotechnol 8:150–154
Raghunathan D (2013) Production of microbial cellulose from the new bacterial strain isolated from temple wash waters. Int J Curr Microbiol App Sci 2:275–290
Rajwade JM, Paknikar KM, Kumbhar JV (2015) Applications of bacterial cellulose and its composites in biomedicine. Appl Microbiol Biotechnol 99:2491–2511. doi:10.1007/s00253-015-6426-3
Ramirez-Flores J, Rubio E, Rodriguez-Lugo V, Castano VM (2009) Purification of polluted waters by functionalized membranes. Rev Adv Mater Sci 21:211–216
Rawlings DE (1995) Restriction enzyme analysis of 16S rDNA for the rapid identification of Thiobacillus ferrooxidans, Thiobacillus thiooxidans, and Leptospirillum ferrooxidans strains in leaching environments. In: Jerez CA, Vargas T, Toledo H, Wiertz JV (eds) Biohydrometallurgical processing, vol II. University of Chile, Santiago, pp 9–17
Rezaee A, Godini H, Bakhtou H (2008) Microbial cellulose as support material for the immobilization of denitrifying bacteria. Environ Eng Manage J 7:589–594
Ross P, Mayer R, Benziman M (1991) Cellulose biosynthesis and function in bacteria. Microbiol Rev 55:35–58, PMCID:PMC372800
Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425
Schramm M, Hestrin S (1954) Factors affecting production of cellulose at the air/liquid interface of a culture of Acetobacter xylinum. J Gen Microbiol 11:123–129. doi:10.1099/00221287-11-1-123
Schrecker ST, Gostomski PA (2005) Determining the water holding capacity of microbial cellulose. Biotechnol Lett 27:1435–1438. doi:10.1007/s10529-005-1465-y
Segal L, Creely JJ, Martin AE Jr, Conrad CM (1959) An empirical method for estimating the degree of crystallinity of native cellulose using the X-ray diffractometer. Text Res J 29:786–794. doi:10.1177/004051755902901003
Shah J, Brown RM (2005) Towards electronic paper displays made from microbial cellulose. Appl Microbiol Biotechnol 66:352–355. doi:10.1007/s00253-004-1756-6
Sheykhnazari S, Tabarsa T, Ashori A, Shakeri A, Golalipour M (2011) Bacterial synthesized cellulose nanofibers: effects of growth times and culture mediums on the structural characteristics. Carbohydr Polym 86:1187–1191. doi:10.1016/j.carbpol.2011.06.011
Shi Z, Zhang Y, Phillips GO, Yang G (2014) Utilization of bacterial cellulose in food. Food hydrocolloid 35:539–545. doi:10.1016/j.foodhyd.2013.07.012
Shoda M, Sugano Y (2005) Recent advances in bacterial cellulose production. Biotechnol Bioprocess Eng 10:1–8. doi:10.1007/BF02931175
Sievers M, Swings J (2005) Family II: Acetobacteraceae. In: Brenner DJ, Krieg NR, Staley JT (eds) Bergey’s manual of systematic bacteriology, vol 2, 2nd edn. Springer, New York, pp 41–96
Smith BG, Harris PJ (1995) Polysaccharide composition of unlignified cell walls of pineapple [Ananas comosus (L.) Merr] fruit. Plant Physiol 107:1399–1409
Soares S, Camino G, Levchik S (1995) Comparative study of the thermal decomposition of pure cellulose and pulp paper. Polym Degrad Stabil 49:275–283. doi:10.1016/0141-3910(95)87009-1
Sun JX, Xu F, Sun XF, Xiao B, Sun RC (2005) Physico-chemical and thermal characterization of cellulose from barley straw. Polym Degrad Stabil 88:521–531. doi:10.1016/j.polymdegradstab.2004.12.013
Surma-ślusarska B, Presler S, Danielewicz D (2008) Characteristics of bacterial cellulose obtained from Acetobacter xylinum culture for application in papermaking. Fibres Text East Eur 16:108–111
Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599. doi:10.1093/molbev/msm092
Tokoh C, Takabe K, Sugiyama J, Fujita M (2002) CP/MAS 13 C NMR and electron diffraction study of bacterial cellulose structure affected by cell wall polysaccharides. Cellulose 9:351–360. doi:10.1023/A:1021150520953
Ul-Islam M, Khan T, Parka JK (2012) Water holding and release properties of bacterial cellulose obtained by in situ and ex situ modification. Carbohyd Polym 88:596–603. doi:10.1016/j.carbpol.2012.01.006
Vandamme EJ, De Baets S, Vanbaelen A, Joris K, De Wulf P (1998) Improved production of bacterial cellulose and its application potential. Polym Degrad Stab 59:93–99. doi:10.1016/S0141-3910(97)00185-7
Wee Y, Kim S, Yoon S, Ryu H (2011) Isolation and characterization of a bacterial cellulose-producing bacterium derived from the persimmon vinegar. African J Biotechnol 10:16267–16276. doi:10.5897/AJB11.2036
Williams WS, Cannon RE (1989) Alternative environmental roles for cellulose produced by Acetobacter xylinum. Appl Environ Microbiol 55:2448–2452
Wu ZY, Li C, Liang HW, Chen JF, Yu SH (2013) Ultralight, flexible, and fire-resistant carbon nanofiber aerogels from bacterial cellulose. Angew Chem Int Ed Engl 52:2925–2929. doi:10.1002/anie.201209676
Yamada (2013) List of new names and new combinations previously effectively, but not validly, published. Int J Syst Evol Microbiol 63:1–5. doi:10.1099/ijs.0.049312-0
Yamada Y, Yukphan P, Lan Vu HT, Muramatsu Y, Ochaikul D, Tanasupawat S, Nakagawa Y (2012) Description of Komagataeibacter gen. nov., with proposals of new combinations (Acetobacteraceae). J Gen Appl Microbiol 58:397–404. doi:10.2323/jgam.58.397
Yang Y, Jia J, Xing J, Chen J, Lu S (2013) Isolation and characteristics analysis of a novel high bacterial cellulose producing strain Gluconacetobacter intermedius CIs26. Carbohydr Polym 92:2012–2017. doi:10.1016/j.carbpol.2012.11.065
Zakaria J, Nazeri MA (2012) Optimization of bacterial cellulose production from pineapple waste: effect of temperature, pH and concentration. In: EnCon 2012, 5th engineering conference, “Engineering towards change — empowering green solutions,” 10–12th July 2012, Kuching, Sarawak
Zhang T, Wang W, Zhang D, Zhang X, Ma Y, Zhou Y, Qi L (2010) Biotemplated synthesis of gold nanoparticle-bacteria cellulose nanofiber nanocomposites and their application in biosensing. Adv Funct Mater 20:1152–1160. doi:10.1002/adfm.200902104
Zhang X, Fang Y, Chen W (2013) Preparation of silver/bacterial cellulose composite membrane and study on its antimicrobial activity. Synth React Inorganic Met Nano-Metal Chem 43:907–913. doi:10.1080/15533174.2012.750674
Zhu H, Jia S, Yang H, Tang W, Jia Y, Tan Z (2010) Characterization of bacteriostatic sausage casing: a composite of bacterial cellulose embedded with ε-polylysine. Food Sci Biotechnol 19:1479–1484. doi:10.1007/s10068-010-0211-y
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JVK is thankful to CSIR, Govt. of India, New Delhi for providing research fellowship. Authors acknowledge financial support from DST, Govt. of India, New Delhi for carrying out the research.
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Kumbhar, J.V., Rajwade, J.M. & Paknikar, K.M. Fruit peels support higher yield and superior quality bacterial cellulose production. Appl Microbiol Biotechnol 99, 6677–6691 (2015). https://doi.org/10.1007/s00253-015-6644-8
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DOI: https://doi.org/10.1007/s00253-015-6644-8