Flores Lugo, J. A., Flores García, A. L., Torres Portillo, M. D., Avila Mascareño, M. F., Cota García, K. P., Martínez Vidales, A. D., Parra Cota, F. I. & Santos Villalobos, S. S. (2022). Celulosa bacteriana: una alternativa promisoria para diversificar la producción de papel de manera sostenible. Revista investigaciones y estudios – UNA, 13(2), 59-75. https://doi.org/10.47133/IEUNA22206b

Abstract. Global environmental changes related to anthropogenic activities are becoming increasingly common. Currently, there are multiple environmental problems caused by human production systems, which require more sustainable alternatives to reduce and/or mitigate their negative impact on the environment, highlighting activities such as tree felling. Vegetable cellulose (obtained mainly from trees) is a raw material of great importance in manufacturin of paper; therefore, the future of forests depends on the manufacture and consumption of paper. The present review analyzes the use of bacterial cellulose as a raw material for substituting vegetable cellulose in the paper industry for a possible reduction of tree felling.

Keywords. bacterial cellulose, papermaking, biotechnology, environmental issues.

Resumen. Los cambios ambientales globales relacionados con las actividades antrópicas son cada vez más comunes. En la actualidad, existen múltiples problemas ambientales provocados por los sistemas de producción humanos, los cuales, requieren de alternativas más sostenibles para reducir y/o mitigar su impacto negativo en el medio ambiente, destacando actividades como la tala de árboles. La celulosa vegetal (obtenida principalmente de los árboles) es una materia prima de gran importancia en la fabricación de papel; por lo que el futuro de los bosques depende de la fabricación y el consumo de papel. La presente revisión analiza el uso de la celulosa bacteriana como materia prima para la sustitución de la celulosa vegetal en la industria papelera para una posible reducción de la tala de árboles.

Palabras clave. celulosa bacteriana, fabricación del papel, biotecnología, problemas ambientales.

INTRODUCCIÓN

Currently, it is possible to observe diverse environmental problems around us, such as deforestation, which is carried out for multiple purposes, primarily for paper manufacture. For centuries humans have used fibrous raw material to make paper. (Area, 2008). The paper and related products are made from cellulose, the main component of plant cell walls. This cellulose can come from various plants, such as cotton, wood, cereal straw, and sugar cane, among others (Area, 2008), although most papers are made from cellulose from wood (Lera Santín, 2011).

Trees are of major environmental importance since they host many species (birds, insects, mammals); in addition to photosynthesis, providing oxygen, and absorbing carbon dioxide. Furthermore, they help regulate the planet's climate and prevent soil erosion. Deforestation is a severe problem and one of the leading causes of habitat destruction, causing biodiversity loss, and negative changes in carbon dioxide (CO₂) fixation. In deforesting regions, the soil is affected by erosion and is frequently degraded to non-productive lands. Considering all these negative environmental impacts, there is a promising solution, which consists of using bacterial cellulose obtained from microorganisms. Bacterial cellulose, like plant cellulose, is an insoluble extracellular polymer that is produced by a variety of bacterial species within the genera Achromobacter, Agrobacterium, Rhizobium, Sarcina, Zoogloea, and Gluconacetobacter (Chávez-Pacheco et al., 2004). Gluconacetobacter xylinus (formerly Acetobacter xylinum) is a Gram-negative bacterium, strictly aerobic, that performs incomplete oxidation of several sugars and alcohols (a process known as oxidative fermentation). Its natural ecological niche is decomposing fruits and vegetables, and it can produce bacterial cellulose on liquid and solid media by forming a film on the surface (Chávez-Pacheco et al., 2004). The cellulose synthesized by G. xylinus is structurally and chemically the same as the plant cellulose; however, the bacterial cellulose is found with high purity, free of lignin and hemicellulose, and has a high capacity for water absorption and mechanical resistance. Cellulose fibers synthesized by bacterial cellulose are much smaller than wood fibers (Chávez-Pacheco et al., 2004). These peculiarities make bacterial cellulose a feasible material for papermaking.

Conventional paper manufacturing

In papermaking there are multiple production methods, previously the most popular was mechanical abrasion and the application of chemicals based on caustic soda, sulfites, and sulfates. Currently, the most widely used methods are the mechanical and the Kraft method (based on sodium hydroxide and sodium sulfide) (Boeykens, 2006; Mues et al., 2018).

The paper-making process begins with the treatment of raw material by debarking and shredding the wood to obtain the cellulose. Then, the pulp is prepared, depending on the type of tree it came from: i) chemical treatment in which the wood previously converted into small chips is passed through a cooking process with chemical products, for example, the kraft treatment for resinous trees of Evergreen, currently one of the most used (Boeykens, 2006), covering approximately 72% of the world's cellulose production, this process generates a large amount of waste that is difficult to biodegrade and has use of 60% (Mues et al., 2018); and ii) mechanical process for trees of expired leaf, this method represents 20% of world production, which requires significant energy consumption and its use is 90 to 98% to obtain pulp (Mues et al., 2018). The composition of the wood is complex. Cellulose is the cell wall's basic structural element and is accompanied by lignin and hemicellulose.. It gives it a dark brown coloration, for that reason, it requires a bleaching process. In this stage can be used different bleaching agents like hydrogen peroxide (which changes the structure of lignin altering the color, but does not eliminate it), chlorine, hypochlorite, or chlorine dioxide, which generates toxic waste, in addition, the treatment of water after bleaching (Boeykens, 2006; Mues et al., 2018; Merizalde et al., 2019). At this point the cellulose pulp has high water content, so it is deposited in a machine where it is transferred on a long belt driven by rollers, then, the water is removed by different procedures, like gravity, vacuum, pressure, and drying. And finally, a massive sheet of paper is obtained, which is rolled up to form a bovine (Figure 1) (Mues et al., 2018).

The function of the bcsC gene and the bcsD gene has not yet been discovered. However, it is proposed that the bcsC gene functions as a 3.5 nm pore-forming protein, which is diametrically aligned in the cell membrane to allow cellulose secretion. In contrast, the bcsD gene appears to be involved in controlling the crystallization process of cellulose nanofibrils (Liu et al., 2018b). Besides, it is hypothesized that the bcsD gene is found extracellularly and that its function is to twist the newly synthesized cellulose fibrils, generating higher-order fibers, which would explain why G. xylinus produces fibrillar cellulose and other bacteria that lack the bcsD gene produce amorphous cellulose (Prada Ramírez, 2014).

Recently, Kubiak et al., (2014) identified the orf2 whose function is still unknown, and the bcsZ gene that encodes an endo-β-(1-4)-glucanase whose function is to divide the bacterial cellulose chains, consequently, more chains are generated and when these are joined microfibrils are formed. Finally, located downstream (3') of the cellulose synthase operon there is a gene that encodes a β-glucosidase, which hydrolyzes glucose units formed by more than three monomers and plays an important role in cellulose production and the microfibril packaging produces the cellulose fibers and ribbons (Figure 4) (Schmid et al., 2015) which reach a thickness of 1 to 9 µm and form an extensive reticulated structure stabilized by hydrogen bonds, the condensation of the tapes gives rise to the three-dimensional structure or macrostructure of the bacterial cellulose (Gorgieva & Trček ,2019).

Production of bacterial cellulose

The production of bacterial cellulose strictly depends on the growth medium, which can be static or agitated. Furthermore, it influences the sources of carbon, nitrogen, pH, temperature, availability of oxygen, minerals, the proportion of the inoculant, and finally the age that the inoculum present (Santos et al., 2016; Aswini et al., 2020). In the CB production industry, it is common to use molasses obtained from sugar cane as a carbon source. In addition, different additives are used to increase its production (Table 5). These additives can be glycerol, sodium alginate, ethanol, etc. among others (Gorgieva & Trĉek, 2019).

Currently, there are different methods to produce bacterial cellulose, some of them can be obtained through shaken, static cultures or grown in bioreactors (Wang et al., 2019). When static media are used, there is usually a uniform cellulose layer i.e., a film is formed between the liquid and air phase of the culture, the purpose of cellulose synthesis is to supply a firm surface matrix, which allows the microorganism, a strictly aerobic, to be close to the gas phase (Carreño Pineda et al., 2012); in the case of shaken cultures or agitation, cellulose usually appears in the form of clusters or masses in an irregular manner (Tuya Salas et al., 2021). The production of bacterial cellulose through the use of agitated cultures is more advisable for the industry since a greater production is obtained (due to greater availability of oxygen), however, this technique usually presents a low level of polymerization and has a higher crystallization characteristic when compared to static culture (Lahiri et al., 2021; Gorgieva & Trĉek, 2019).

Reactors used in the production of bacterial cellulose

As mentioned, bacterial cellulose can be produced by a) bioreactors called airlift and b) trickling bed.The first (a) presentssufficient oxygen with a reduced feed source, resulting in cellulose in pelletized form. The second (b) has a high availability of oxygen but at a decreased shear strength, where the product can be found in irregular leaves (Gorgieva & Trĉek, 2019).On the other hand, there is a so-called rotating disk reactor, which consists of a series of circular disks mounted on the horizontal axis that rotate and are alternately exposed to the fermentation environment and the air. The cellulose obtained in the reactor does not face strong shear stress and has excellent oxygen transmissibility, so microorganisms can easily come into contact with it. Thus, the production of bacterial cellulose by Gluconacetobacter xylinus was maximized at 5.52 g/L; In addition, constant aeration improve production, reaching a production of 5.67 g/L (Guinea Nava, 2016).

Valuation of trees, water pollution, and soil los

Carbon dioxide (CO₂) is the primary anthropogenic greenhouse gas (GHG) in the atmosphere, it contributes approximately 65% to the radiative forcing produced by long-lived GHGs (National Oceanic and Atmospheric Administration [NOAA], 2016).

Of the total emissions from human activities during the period 2006-2015, about 44% were stored in the atmosphere, 26% in the oceans, and 30% on land. One way to reduce the effects of CO₂ is to store it in the biomass through photosynthesis, considering that the potential for carbon capture by plant communities varies according to their structure and the constitution of each ecosystem (Jiménez Pérez et al., 2020)

Since the end of the of the last century, Central American countries carbon fixation and capture capacity have been evaluated to measure their potential for the mitigation of Greenhouse Gases (GHG) caused by growing industrial activity (López et al. 2018). Forest plantations have become a strategic means of fixing atmospheric CO₂ in the plant structure. In the paper industry, the prices of a ton of fixed C vary between $ 4.6 - 50.4 US, depending on the actual discount rates and the amount of C added to that obtained in the traditional wood business (Gutiérrez Velez & Lopera Arango, 2001).

The absorption potential of the forestry sector in Mexico has been estimated at 58 million tons of carbon dioxide equivalent (t CO2e) by 2020 and 96 million tons of CO2e by 2030 (Coordinación General de Producción y Productividad de la Comisión Nacional Forestal [CONAFORT], 2013). For Mexico, in 2014, 137.8 million hectares of forest area were counted, representing 70.5% of the 196.5 million hectares of the national territory. México wood production is insufficient to satisfy the internal demand. In 2016, 6.71 million m³ of round wood was produced (29% of the total volume), with an apparent consumption of 23.4 million m³. Of the 6.71 million m³ of wood, different classes of wood products were obtained where cellulose represents a total of 0.61 million m³ (9.2%); however, from 1997 to 2016, a decreasing trend of cellulose was registered with an average annual rate of -3.50% (Centro de Estudios para el Desarrollo Rural Sustentable y la Soberanía Alimentaria [CEDRSSA], 2019). Even so, a representative amount of the country's forest area continues to be deforested, with 9.2% going to the production of this cellulose.

20% of the wood used in papermaking comes from original natural forests and 29% from plantations, and 54% from secondary forest (Greenpeace, 2004). Plantation forests are increasing rapidly in the world to alleviate deforestation and degradation of natural forests, along with providing goods and services. Monoculture plantations have been the dominant type of plantation in practice and are well-recorded in research, a higher diversity of tree species increases the number of ecological niches, which can further increase the number of associated species, loss of soil productivity and fertility, disruption of hydrological cycles, risks associated with plantation forestry practices (e.g., the introduction of exotic species), risks of promoting pests and diseases, higher risks of adverse effects of storms and fire, and negative impacts on biodiversity (Liu et al., 2018b).

In the paper industry, in addition to the problem of deforestation, there is high consumption of water, energy, and chemical substances that can lead to the contamination of water sources and air (Romero Conrado et al., 2017). Water is one of the key components of papermaking; paper production is unthinkable without water. The pulp and paper industry is ranked as the world’s third-largest water consumer and produces high amounts of wastewater. In 2019, the total use of water in Spanish pulp and paper mills stood at 111 million m3 per year, which is half the water of water than in 1990 and 30% less than in 2000, while production has increased by 60% since the beginning of the nineties and 22% since the beginning of the XXI century (Carpintero, 2019). It is worth mentioning that the paper industry has improved its processes in the last few decades and as a result, has been able to reduce its water consumption significantly. For the last several years the paper industry has been working to reduce its freshwater consumption and its wastewater output. Reuse is an important approach for reducing wastewater generation and consumption of wastewater, however, the process is still carried out mainly from water from rivers 69%, from wells 19% and only from the network, and recovered water 12% (Carpintero, 2019).

Thanks to the voluntary agreement signed between the Ministry of the Environment and the Association of Pulp and Cardboard Manufacturers (ASPAPEL) during the years 2000-2009, marked a fundamental milestone in the efficiency of water use and discharges in the sector, achieving a 37% reduction in the use of water per ton produced (from 24.5 m3/t to 15.5 m3/t) and a 28% reduction in the use of total water (going from 160 cubic hectometers/year to 115 cubic hectometers/year), despite an increase in production of 14% in the same period. To reduce water consumption, the Spanish paper industry requires a powerful investment effort (almost 1,400 million euros of investment in the last four years alone), to reduce environment effects(Carpintero, 2019).

The importance of soil losses can be focused on the services it provides, like “filtering of nutrients and contaminants”, the economic cost numbers based on estimations of nitrate unit damage, based on the soil retention and the unit damage cost, were in the range 0–280 id$ ha^-1 year^-1. For the service of “climate regulation” the total average cost of reducing greenhouse gas emissions under the Mitigation Scenarios is estimated at between €190 and €240 tons of CO2 (2008 prices), and for “biomass production” the grassland, shrubland, and pasture cost 740 id$ha^-1 year^-1 (270–1580); non-irrigated arable land 2230 id$ha^-1 year^-1 (440–4730); fruit and berry plantations cost 7500 id$ha^-1 year^-1 (6100–7580); and Olive groves 10,810 id$ha^-1 year^-1 (6540–10,910) (Jónsson et al., 2017). Soil can have or provide other important goods and services, maintenance is, therefore, essential to achieve environmental and economic sustainability.

Comparison of paper production costs with plant cellulose vs. bacterial cellulose

Bacterial cellulose represents the purest form of cellulose, and it possesses several unique properties. Despite its impressive potential for a wide range of commercial applications, bacterial cellulose is prohibitively expensive to manufacture. This high cost limits its use as an alternative to plant cellulose. The synthetic media commonly used for this kind of cellulose production are the major factor contributing to its high production cost. Therefore, efforts have been made to devise strategies for the effective and inexpensive production of bacterial cellulose, these include testing various waste materials such as fruit juices, industrial wastes, and food wastes (Islam et al., 2017). The cost of the carbon source plays a key role in bacterial cellulose production costs. Low-cost carbon sources such as glycerol must be obtained as a byproduct of biodiesel production, and grape bagasse from regional wine production for example. The volumetric productions (g/l) and the yield (g/g) of bacterial cellulose in a culture medium by replacing glucose with other carbon sources show that the production of this type of cellulose with glucose has a cost of 0.22-0.24 U$D/kg, the cane molasses of 0.12 U$D/kg, commercial glycerol 0.46-0.75 U$D/kg and glycerol from biodiesel 0.04-0.15 U$D/kg (Vázquez et al., 2013).

In Latin America with a volume produced of 6,152 thousand tons of cellulose, there are profits of 1,486 million dollars. Between 2002 and early 2008, the price of pulp increased from $350 to $755 per ton, an increase of 116%. From the second semester of 2008, the price of cellulose started to fall, reaching 475 dollars at the beginning of 2009, that is, a fall of 37% (Chapela, 2012).

CONCLUSIONS

Papermaking has caused several negative impacts on the environment derived from deforestation, such as habitat loss, biodiversity, soil erosion, and reduction of carbon dioxide (CO2) fixation, thus suggesting the need to develop sustainable alternatives to counteract these impacts, one of these alternatives is bacterial cellulose.

Gluconacetobacter xylinus has great similarities with plant cellulose (used for papermaking). It has been determined that bacterial cellulose is structurally and chemically equal to plant cellulose, however, it has better characteristics (high purity, high water absorption capacity and mechanical resistance, and high degree of polymerization) which makes it a feasible alternative for paper manufacturing, avoiding environmental damage caused by the processes of paper production, mainly deforestation, debarking, screening, and bleaching. Therefore, the knowledge of the growth conditions of G. xylinus, its metabolism, formation, and excretion of bacterial cellulose, and the structure of the synthesized cellulose, is decisive in knowing which reactor to use to achieve maximum production of bacterial cellulose.

Despite its great potential as an alternative to plant cellulose for papermaking, producing bacterial cellulose is expensive; however, we must measure what conventional paper manufacturing costs environmentally. Although the manufacture of paper with plant cellulose is indeed more economical, this leads to severe impacts on the environment. Therefore, it is considered necessary to continue making efforts to design strategies for the economical production of bacterial cellulose and to achieve sustainable paper manufacturing.

ACKNOWLEDGMENTS

The authors acknowledge support from the project PROFAPI 2022_0001.

SOURCE OF FINANCING. No external financing.

Competing interests. The authors have declared that no competing interests exist.

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Agents	The concentration of the agent (%)	pH	Consistency (%)	Temperature (°C)	Time (h)
Chlorine	2.5-8	2	3	20-60	0.5-1.5
Sodium hydroxide (NaOH)	1.5-4.2	11	10-12	<80	1-2
Chlorine dioxide (ClO₂)	1	0-6	10-12	60-75	2-5
Sodium hypochlorite (NaOCl)	1-2	9-11	10-12	30-50	0.5-3
Oxygen (O₂₎	1.2-1.9	7-8	25-33	90-130	0.3-1
Hydrogen Peroxide (H₂O₂)	0.25	10	12	35-80	4
Ozone (O₃)	0.5-3.5	2-3	35-55	20-40	<0.1
Sulfur dioxide (SO₂)	4-6	1.8-5	1.5	30-50	0.25
Sodium dithiosulfure (NaS₂O₄)	1-2	5.5-8	4-8	60-65	1-2

Raw material	1-ton paper	500 virgin fiber foils	Recycled paper
Water	150,000 a 200,000 L	130. 6 L	2,000 L
Energy	7.000 kW/ h	26,8 kW/h	2 750 kW/h

Properties		*Plant cellulose*	Bacterial Cellulose
Composition % (1)	Cellulose	43-47 (1)	98 (1)
	Lignin	16-24 (1)	0 (1)
	Hemicellulose	23-35 (1)	0 (1)
	Extract	2-8 (1)	0 (1)
Degree of polymerization		13,000-14,000 (2)	2,000-6,000 (2)
Fiber width		1.4-4.0 mm (2) 200–300 MPa	70-80 nm (2)
Water content %		60 (2)	98.5 (2)
Crystallinity %		56-65 (2)	65-79 (2)
Young’s modulus		5.5-12.6 GPa (2)	15-30 GPa (2)
Toxicity		0 (3)	0 (1)

Genera	Cellulose structure
Acetobacter	An extracellular film composed of tapes
Achromobacter	Fibrils
Aerobacter	Fibrils
Agrobacterium	Short fibrils
Alcaligenes	Fibrils
Pseudomonas	Non-distinguishable fibrils
Rhizobium	Short fibrils
Sarcina	Amorphous cellulose
Zoogloea	Not well defined