© The Authors, 2021, Published by the Universidad del Zulia*Corresponding author: odracirhema@gmail.com
Fungal microbiota of sugarcane straw and their ability to produce hydrolytic enzymes
Microbiota fúngica de paja de caña de azúcar y su capacidad para producir enzimas hidrolíticas
Microbiota fúngica de palha de cana-de-açúcar e a sua capacidade de produzir enzimas hidrolítica
Nadia G. Mendoza-Infante
1
Héctor Debernardi de la Vequia
1
Juan V. Hidalgo-Contreras
1
Violeta Mugica-Álvarez
2
Ricardo Hernández-Martínez
3
*
Rev. Fac. Agron. (LUZ). 2022, 39(1): e223908
ISSN 2477-9407
DOI: https://doi.org/10.47280/RevFacAgron(LUZ).v39.n1.08
Crop Production
Associate editor: Ing. Agr. MSc. Evelin Perez
1
Colegio de Postgraduados-Campus Córdoba, Carretera
Federal Córdoba-Veracruz Km 348, Congregación Manuel
León, Municipio Amatlán de los Reyes, 94946 Veracruz,
México.
2
Química Aplicada, Universidad Autónoma Metropolitana,
Unidad Azcapotzalco, Av. San Pablo 180, 02200 México,
DF, México.
3
CONACYT-Colegio de Postgraduados-Campus Córdoba,
Carretera Federal Córdoba-Veracruz Km 348, Congregación
Manuel León, Municipio Amatlán de los Reyes, 94946
Veracruz, México.
Received: 30-03-2021
Accepted: 30-06-2021
Published: 15-12-2021
Abstract
The microbiota presents in sugarcane (Saccharum ofcinarum L.) straw
can have benets to produce sustainable crops, also can be used for the
development of alternative processes to produce molecules of industrial
interest and valorization of biomass and residues unexploited. Therefore,
the objective of the present work was the isolation of the fungal microbiota
present in the sugarcane straw (CP 72-2082) and its capacity to produce
hydrolytic enzymes. The fungal microbiota was isolated by sampling for four
months one sampling for month the straw in elds of the “El Potrero” sugar
mill in the Veracruz state, Mexico, and soil was also sampled to determine
the effect of straw chili on the organic matter content. Furthermore, the
capacity of the strains to produce xylanases and cellulases was determined
in a Petri dish using birch xylan and carboxymethylcellulose as substrates.
Thirty-four strains were isolated from the samples, in all was identied the
genera Trichoderma, Fusarium in three and Aspergillus and Penicillum
in two. The results indicate that if sugarcane straw is reincorporated into
soils where sugarcane is grown, it can have a benecial impact, 22 isolated
strains showed the ability to produce hydrolytic enzymes. The organic matter
content in the soils with both shredded and unshredded crop residues showed
that chili does not present a benet to the soil but can contribute benecial
fungal microbiota for various purposes.
Keywords:
Saccharum ofcinarum
Trichoderma
Fungus
Cellulases
Xylanases
This scientic publication in digital format is a continuation of the Printed Review: Legal Deposit pp 196802ZU42, ISSN 0378-7818.
Rev. Fac. Agron. (LUZ). 2022, 39(1): e223908. January - March. ISSN 2477-9407.
2-6 |
Resumen
La microbiota presente en la paja de caña de azúcar (Saccharum
ofcinarum L.) puede tener benecios para la producción de cultivos
sostenibles, también, puede utilizarse en el desarrollo de procesos
alternos que permitan producir moléculas de interés industrial y
al mismo tiempo valorizar biomasa y residuos no aprovechados.
El objetivo del presente trabajo fue aislar la microbiota fúngica
presente en la paja de caña de azúcar (CP 72-2082) y su capacidad
para producir enzimas hidrolíticas. La microbiota fúngica fue aislada
muestreando una vez por mes durante cuatro meses la paja en campos
del ingenio “El Potrero” en el estado de Veracruz, México, también
se muestreó suelo para determinar el efecto del ahile de la paja
sobre el contenido de materia orgánica. Asimismo, se determinó la
capacidad de las cepas para la producción de xilanasas y celulasas en
caja Petri utilizando xilano de abedul y carboximetilcelulosa como
substratos. En los cuatro muestreos realizados, se aislaron 34 cepas,
identicándose en todos, el género Trichoderma, Fusarium en tres de
ellos y Aspergillus y Penicillum en dos. Los resultados indican que
la reincorporación de la paja de caña en los suelos donde es cultivada
caña de azúcar puede tener impacto benéco, encontrándose que
22 de las cepas aisladas, mostraron la capacidad de producción de
enzimas hidrolíticas. El contenido de materia orgánica, en los suelos
donde se tenían residuos de cosecha ahilados y no ahilados, demostró
que el ahile no presenta un benecio al suelo, pero puede aportar
microbiota fúngica benéca para diversos objetivos.
Palabras clave: Saccharum ofcinarum, Trichoderma, hongos,
celulasas, xilanasas.
Resumo
A microbiota presente na palha da cana de açúcar (Saccharum
ofcinarum L.) pode ter benefícios para a produção de culturas
sustentáveis, e também pode ser utilizada para o desenvolvimento de
processos alternativos para produzir moléculas de interesse industrial
e valorização da biomassa e dos resíduos não explorados. Portanto,
o objectivo do presente trabalho foi o isolamento da microbiota
fúngica presente na palha da cana de açúcar (CP 72-2082) e a sua
capacidade de produzir enzimas hidrolíticas. A microbiota fúngica
foi isolada por amostragem uma vez por mês durante quatro meses
a palha nos campos do moinho de açúcar “El Potrero” no estado de
Veracruz, México, e o solo também foi amostrado para determinar
o efeito da palha chili sobre o conteúdo de matéria orgânica. Além
disso, a capacidade das estirpes para produzir xilanases e celulases
foi determinada numa placa de Petri, utilizando carboximetilcelulose
e xilan de bétula como substratos. Nas quatro amostragens realizadas,
foram isoladas 34 estirpes, identicando o género Trichoderma em
todas elas, Fusarium em três delas e Aspergillus e Penicillum em
duas delas. Os resultados indicam que se a palha da cana de açúcar
for reincorporada em solos onde a cana de açúcar é cultivada, pode
ter um impacto benéco. Além disso, 22 estirpes isoladas mostraram
a capacidade de produzir xilanases e celulases. O teor de matéria
orgânica nos solos com resíduos de culturas triturados e não triturados
mostrou que a pimenta não apresenta um benefício para o solo, mas
pode contribuir com microbiota fúngica benéca para vários ns.
Palavras-chave: Saccharum ofcinarum, Trichoderma, fungos,
celulases, xilanases.
Introduction
From an economic and social point of view, nowadays the
cultivation of sugar cane is the most important in Mexico, since it
contributes 0.5% of the gross domestic product and is present in 15
states of the country (Cervantes-Preciado et al., 2019). Similarly,
according to the Comité Nacional Para el Desarrollo Sustentable para
la Caña de Azúcar (CONADESUCA, 2019), 57,036,700 t of sugar
cane were harvested per hectare during the 2018-2019 harvest.
There is a need to increase the productivity of the cultivation of
sugarcane (Saccharum ofcinarum L.) in a sustainable way, which has
promoted the development of alternatives to improve crop yield, with
the microbiota being a potential option that can allow the exploration
of untapped diversity to modulate growth, development, defense
against pathogens, nutrient acquisition and resistance to stress,
as well as its use in industrial processes for the generation of new
products (De Souza et al., 2016 ). It is currently known that the native
microora of sugarcane is diverse and can benecially inuence its
development and health, such information invites the use of microbial
and industrial technologies for its correct exploitation (Armanhi et
al., 2018; De Souza et al. , 2016). For this reason, the objective of the
present research work is to generate information on the diversity of
fungal strains present in aligned sugarcane straw in sugarcane elds,
in addition to evaluating the potential of these strains for hydrolytic
enzymes production.
Materials and methods
Sampling and harvesting of sugarcane straw
The sugarcane straw (harvest residues), variety CP 72-2086 were
sampled by the practice of align in elds of “El Potrero” sugar mill
in the state of Veracruz. The sampling was carried out using the ve
of golds method (Martínez et al., 2013) taking six samples per point
(identied with a Garmin® GPS) with and without align to compare
the content of organic matter (OM) and pH in soil. The sampling
coordinates were: Point one: Latitude: 18°54’4.93”N, Longitude:
96°46’58.55”W, Point two: Latitude: 18°
54’5.69”N, Longitude:
96°46’56.64”W, Point Three: Latitude: 18°54’11.48”N, Longitude:
96°46’54.80»W, Point Four: Latitude: 18°54’11.95”N, Longitude:
96°46’57.04»W, Point 5: Latitude: 18°54’9.42”N Longitude: 96°
46’56.91”W.
Soil analysis
The soil samples were processed for the determination of organic
matter (OM) by the Walkley-Black method (Yarce and Castillo,
2014). For the determination of OM to 0.5 g of ground soil, 10 mL of
a 1 N solution of potassium dichromate (K
2
Cr
2
O
7
) in acid medium (20
mL of 98 % H
2
SO
4
) were added, after 45 min of In reaction, distilled
water and a few drops of ferroin indicator were added (0.696 g of
ferrous sulfate with 1.485 g of orthophenanthroline monohydrate
(C
12
H
8
N
2
.H
2
O) in 100 mL of distilled water). The quantication was
carried out by titration of Cr
+6
with Mohr’s salt (Fe(NH
4
)
2
(SO
4
)
2
.6H
2
O) 0.5 N. For the determination of pH, dry soil samples were
sieved (2 mm) and 2.5 parts of water were added for each part of soil,
the mixture was allowed to settle and the pH was determined with a
Hanna® potentiometer (Rozas et al., 2011).
Isolation, purication and morphological characterization of
native fungal strains
The fungal strains were isolated by placing small fragments of the
sugarcane straw samples in humid chambers and incubated at 28 °C
for 72 h. The fungal strains were puried by the hyphal tip technique
in the culture medium Dicloran Rosa de Bengal Chloramphenicol
(Millipore®) (Lacerda et al., 2018) and kept at 28 °C for 48 h.
This scientic publication in digital format is a continuation of the Printed Review: Legal Deposit pp 196802ZU42, ISSN 0378-7818.
Mendoza et al. Rev. Fac. Agron. (LUZ). 2022, 39(1): e223908
3-6 |
Once the pure strains were obtained, they were characterized
morphologically (macroscopically and microscopically) by staining
with cotton blue (Merck®), identifying them according to the Barnett
and Hunter guide (1972). Strain purication was performed with
samples collected from March, April, May and June 2018.
Strain growth on plate sugarcane straw
Disks of the puried fungal strains were taken and placed in
the center of Petri dishes containing culture medium prepared
with Bacteriological Agar (Bioxon®) at a concentration of 15 g.L
-
1
and sugar cane straw of particle size smaller than 0.595 mm at a
concentration of 13 g.L
-1
and incubated at 28 °C for seven days,
during which radial growth was measured with the help of a vernier
every 12 h (Lizardi-Jiménez et al., 2019).
Plaque xylanase and cellulase production capacity
The fungal strains that grew in the medium supplemented with
cane straw were sown in Petri dishes with culture medium composed
of agar agar (Sigma®), birch xylan and carboxymethylcellulose
(Sigma®) as the only carbon source (Ramírez-Lozano et al., 2016).
The Petri dishes of the fungal strains that showed growth after seven
days at 28 °C were stained with a 0.4 % solution of Congo red
(Merck®) and after 15 min, the cultures were washed with 10 mL
of 1 M NaCl (Fermont®) to reveal the enzyme halo. The enzymatic
activity of xylanase and cellulase were determined by the presence of
a hydrolysis halo (Adesina and Onilude, 2013; Florencio et al., 2012;
Youssef et al., 2016).
Statistical design and analysis
The experimental design was completely randomized blocks
with two blocks (with and without align), two treatments (OM and
pH) and four replications (March, April, May and June). The results
obtained were analyzed by an analysis of variance (ANOVA) using
the Minitab® software (Borges et al., 2012).
Results and discussion
Soil analysis
Regarding the soil analysis, the statistical analysis reected that
there are no signicant differences between treatments (p > 0.05),
however, the furrows that contained cane straw (align) presented an
average pH of 7 and a content of average organic matter of 16 %,
while the rows without the cane straw had an average pH of 6 and
an organic matter content of 14 %. In the treatments with align the
OM increased 2 % with respect to the soil without align and the pH
decreased from 7 with align to 6 without align which is indicative of
the benet of this practice. The result obtained agrees with results
where it has been reported that harvest residues were stable in the
OM content in the soil (Bojórquez-Serrano et al., 2015; Rivera-Cruz
et al., 2017). Likewise, Quiroz and Pérez (2013) reported that the use
of chemical fertilizers caused acidity in the soil, but after ltering
crop residues, the OM and pH content did not show variations. On the
other hand, it has been shown that harvesting practices that include
burning, generate an appreciable decrease in the OM content in the
long term, which is considered an aspect to control to prevent soil
degradation (Graham et al., 2002), making the disposal of sugarcane
harvest residues even more relevant.
Isolation and characterization of fungal strains
Thirty-four fungal strains were isolated from the sugarcane straw
samplings in March, April, May and June. The results indicated that in
the March sampling, strains of the genera Fusarium and Trichoderma
were isolated, in April Fusarium, Trichoderma and Penicillum, in
May Trichoderma, Penicillum and Aspergillus and in June Fusarium,
Trichoderma, Penicillum and Aspergillus. The results obtained in the
present work show that as the age of the plant increased, a greater
number of fungal genera were isolated, this result agrees with that
reported by Deshmukh et al. (2013) who indicated that the microbial
activity of the plant increases as its age increases.
Figure 1 shows different representative morphological structures
(macroscopic and microscopic) for each fungal strain isolated
and characterized by month of sampling. Likewise, it is important
to mention that the predominated genus in the four samplings was
Trichoderma spp., Followed by Fusarium spp. and Penicillum spp.,
which were detected in three of the four samplings carried out.
Figure 1. Morphological representation of the isolated strains of cane straw Fusarium spp. a) mycelium, b) oval conidia and septa;
Trichoderma spp. c) cottony mycelium, d) hyaline conidiophores and ovoid conidia; Penicillum spp. e) mycelium and spores, f)
branched hyaline conidiophores and globose conidia; Aspergillus spp. e) cottony mycelium and spores, f) hyaline conidiophores and
conidia with globose vesicle.
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Rev. Fac. Agron. (LUZ). 2022, 39(1): e223908. January - March. ISSN 2477-9407.
4-6 |
Strains of Fusarium spp. Isolated (gure 1a) presented white
cottony hyphal growth, while the microscopic structure (gure 1b)
showed extensive septate mycelium, simple conidiophores and oval
conidia, these results agree with the macroscopic and microscopic
structures reported for this fungal strain (Elias et al., 2016; Hsuan
et al., 2011; Upadhyay et al., 2020). On the other hand, the strains
of Trichoderma spp. (gure 1c) isolated showed greenish yellow
cottony mycelial development, while in the microscopic structure
(gure 1d) it showed hyaline conidiophores and ovoid conidia,
these results agree with the macroscopic and microscopic structures
reported by various authors (Kannangara and Dharmarathna 2017;
Tegene et al., 2021). Strains of Penicillum spp. presented green
cottony hyphal growth with diffusible pink pigmentation (gure
1e) with moderate sporulation, these characteristics are similar to a
strain of Penicillum sp. characterized by Dhakar et al. (2014), on the
other hand, the microscopic structure (gure 1f) showed branched
hyaline conidiophores and globose conidia, characteristics similar
to those reported by various authors (Dhakar et al., 2014; Saif et
al., 2020). Lastly, the Aspergillus spp. isolates presented aerial
mycelium with abundant sporulation and black spores (gure 1g)
and the microscopic structure presented hyaline conidiophores and
conidia with globose vesicle, these results coincide with what was
indicated by Batista-García et al. (2014) for Aspergillus sp. cane
bagasse isolated.
Romão-Dumaresq et al. (2016), indicated that the fungal
community of the sugarcane rhizosphere contains at least 35
different species, in which the presence of the genera identied in
the present investigation predominates. Trichoderma is known as
an antagonist that can act as a controller of red rot (Collecotricum
falcatum) in sugar cane and, its presence in soils has favored
germination, yield and, therefore, its presence in cane straw. of
sugar sampled may represent an opportunity to reintegrate it into
the soils where sugar cane is produced (Joshi et al., 2016).
Studies with Fusarium spp. indicate that it is considered a
phytopathogenic endophyte (Bertonha et al., 2018) and is associated
with the disease known as red rot, which causes the inversion of
sucrose reducing yields (Dela-Cueva et al., 2019), although it is
also has indicated the resistance of sugarcane to this fungal strain
(Mahlanza et al., 2013), so its presence can cause this disease in
sugarcane stems, which is why careful handling of harvest residues.
However, like Trichoderma, Fusarium is a strain that has been
shown to be useful for the production of hydrolytic enzymes,
however, as it is a phytopathogen, more studies are required to
guarantee or rule out its use for this purpose.
Finally, there is research on the isolation of Aspergillus spp.
and Penicillum spp. of sugar cane residues, mainly bagasse, which
is attributed the capacity to produce hydrolytic enzymes, such as
xylanases and cellulases (Agudelo et al., 2013; Batista-García et
al., 2014), so its presence in crop residues does not represent any
risk.
Growth on sugarcane straw in plate
On the other hand, the results of growth in a Petri dish
supplemented with sugarcane straw showed that of the 34 isolated
strains, 23 grew on the straw (as the only carbon source), indicating
that the strains have the ability to incorporate nutrients from
sugarcane straw to its metabolism and produce hydrolytic enzymes
(Marques et al., 2018), so they can be used to design a solid state
cultivation system for the production of xylanases and cellulases
using cane straw of sugar as a substrate.
Plaque xylanase and cellulase production capacity
The strains that grew on the sugarcane straw were subjected to
qualitative tests for the production of xylanases and cellulases in
a Petri dish on birch xylan and carboxymethylcellulose. Of the 23
strains used in the test, 22 had the ability to grow on birch xylan, of
which 8 were from the genus Fusarium (gure 2B c and d), 11 from
Trichoderma (gure 2A a and b) and 3 from Penicillum (gure 2C e
and f), the latter showed little growth as well as the hydrolysis halo.
On the other hand, 22 strains grew on carboxymethylcellulose, 8
from the
Fusarium genus (Figure 3B c and d), 12 from Trichoderma
(Figure 3A a and b) and 2 from Penicillum (Figure 3C e and f).
The strains corresponding to the Trichoderma genus with growth
capacity on birch xylan and carboxymethylcellulose, showed their
potential to produce extracellular xylanases and cellulases, as can
be seen in gures 2 and 3 where it is observed that they formed a
hydrolysis halo in the Petri dishes.
Figure. 2. Growth of the fungal strains on plates supplemented
with birch xylan as the sole carbon source and
the hydrolysis halo revealed with Congo red. A:
Trichoderma spp. a) halo of hydrolysis, b) growth;
B: Fusarium spp. c) halo of hydrolysis, d) growth; D:
Penicillum spp. d) hydrolysis halo, e) growth.
Figure 3. Growth of the fungal strains on plates supplemented
with carboxymethylcellulose as the sole carbon source
and the hydrolysis halo revealed with Congo red.
A: Trichoderma spp. a) halo of hydrolysis, b) growth;
B: Fusarium spp. c) halo of hydrolysis, d) growth; C:
Penicillum spp. d) halo of hydrolysis, e) growth.
This scientic publication in digital format is a continuation of the Printed Review: Legal Deposit pp 196802ZU42, ISSN 0378-7818.
Mendoza et al. Rev. Fac. Agron. (LUZ). 2022, 39(1): e223908
5-6 |
The growth results of Trichoderma spp. on
carboxymethylcellulose and birch xylan demonstrate the potential
of these fungal strains for the production of cellulases and
xylanases, this fungal genus has been recognized for its ability to
produce this type of enzymes extracellularly (Rahnama et al., 2013;
Zhang et al., 2018). For this reason, the sugarcane straw and the
fungal strain can be used for the design of a rational process for the
production of hydrolytic enzymes, where the sugarcane straw can
serve as a substrate and the fungal biomass can be the inoculum
for the production of said enzymes (Farinas, 2015; Florencio et
al., 2015), thus developing an integral process for the use of straw
and native strains. It is very important to highlight that Marques
et al. (2018) published that an endophytic strain of Trichoderma
viridae presented an enzymatic activity of cellulase of 64 Ug
-1
and
xylanase of 351 Ug
-1
in solid culture using cane bagasse as support,
reafrming the possibility of designing a process for the production
of hydrolytic enzymes.
Likewise, investigations in corn harvest remains, indicate that
Fusarium oxysporum (Panagiotou et al., 2003), as well as, in forest
waste Aspergillus niger and F. oxysporum (Kaushal et al., 2012),
have the ability to produce enzymes extracellular hydrolytics.
Therefore, the strains of Fusarium spp. isolated in the present
work, as well as sugarcane straw can be explored for the design of
a process for the production of hydrolytic enzymes in solid culture,
since they showed the growth capacity on carboxymethylcellulose
and birch xylan. In addition, there are reports that indicate that
hydrolytic enzymes can be produced efciently using co-cultures
of Fusarium oxysporum with Aspergillus niger, the second was also
present in the sugarcane straw evaluated (Romão-Dumaresq et al.,
2016).
Finally, it is important to mention that the isolated strains with
morphological characteristics corresponding to Penicillum spp.,
Showed growth on carboxymethylcellulose and birch xylan, so
it can also be explored for the production/design of hydrolytic
enzymes, this species has been reported as part of the sugarcane
rhizosphere (Romão-Dumaresq et al., 2016) and also as a producer
of hydrolytic enzymes (Camassola and Dillon, 2010; Gong
et al., 2015). However, for strains with the ability to produce
hydrolysis halo in plates with culture medium supplemented with
carboxymethylcellulose and birch xylan, as the only carbon source,
additional studies are required in solid culture where the enzymatic
activity is quantied and thus, know the real potential of the strains.
Conclusions
The sugar cane straw align favors that the organic matter content
does not have signicant variations in soils where sugar cane is
grown. While the fungal microbiota isolated from the sugarcane
straw was Trichoderma spp., Fusarium spp., Penicillum spp. and
Aspergillus spp. Furthermore, three of the four isolated fungal
strains showed potential to grow using carboxymethylcellulose and
birch xylan as the sole carbon source indicative of their potential to
produce extracellular hydrolytic enzymes.
Acknowledgment
Mendoza-Infante N. Grace appreciates the scholarship granted
by CONACyT for Master’s studies.
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