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Fungal Deterioration of the Bagasse Storage from the Harvested Sugarcane

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Fungal Deterioration of the Bagasse Storage from the Harvested Sugarcane Peng et al. Biotechnol Biofuels (2021) 14:152 https://doi.org/10.1186/s13068-021-02004-x Biotechnology for Biofuels RESEARCH Open Access Fungal deterioration of the bagasse storage from the harvested sugarcane Na Peng1†, Ziting Yao1†, Ziting Wang1, Jiangfeng Huang1, Muhammad Tahir Khan2, Baoshan Chen1 and Muqing Zhang1* Abstract Background: Sugarcane is an essential crop for sugar and ethanol production. Immediate processing of sugarcane is necessary after harvested because of rapid sucrose losses and deterioration of stalks. This study was conducted to fll the knowledge gap regarding the exploration of fungal communities in harvested deteriorating sugarcane. Experi- ments were performed on simulating production at 30 °C and 40 °C after 0, 12, and 60 h of sugarcane harvesting and powder-processing. Results: Both pH and sucrose content declined signifcantly within 12 h. Fungal taxa were unraveled using ITS ampli- con sequencing. With the increasing temperature, the diversity of the fungal community decreased over time. The fungal community structure signifcantly changed within 12 h of bagasse storage. Before stored, the dominant genus (species) in bagasse was Wickerhamomyces (W. anomalus). Following storage, Kazachstania (K. humilis) and Saccharo- myces (S. cerevisiae) gradually grew, becoming abundant fungi at 30 °C and 40 °C. The bagasse at diferent tempera- tures had a similar pattern after storage for the same intervals, indicating that the temperature was the primary cause for the variation of core features. Moreover, most of the top fungal genera were signifcantly correlated with environ- mental factors (pH and sucrose of sugarcane, storage time, and temperature). In addition, the impact of dominant fungal species isolated from the deteriorating sugarcane on sucrose content and pH in the stored sugarcane juice was verifed. Conclusions: The study highlighted the importance of timeliness to refne sugar as soon as possible after harvest- ing the sugarcane. The lessons learned from this research are vital for sugarcane growers and the sugar industry for minimizing post-harvest losses. Keywords: Sugarcane biodegradation, Post-harvest storing, Fungal community, Yeast, Sucrose losses Background be processed into sugar quickly after harvested. Te post- Sugarcane is one of the most crucial crops for sugar and harvest deterioration of sugarcane is a severe problem for bioethanol production [1]. Te estimated annual gross the sugar industry, causing 20–30 percent sucrose losses sugar output from sugarcane is valued as high as $76 bil- in cane-producing countries [2–5]. Many factors are lion [2]. Sugarcane is a perishable commodity and must associated with the deterioration of the harvested cane, including cane cultivar and its maturity, mechanical or manual harvesting, exposure to microbes, cut-to-crush *Correspondence: [email protected] delay, and storage [2, 5, 6]. †Na Peng and Ziting Yao contributed equally to this paper Te sugar industry prefers pre-harvest sugarcane 1 Guangxi Key Laboratory for Sugarcane Biology & State Key Laboratory for Conservation and Utilization of Subtropical Agro-Bioresources, burning during sugarcane harvesting globally because Guangxi University, Nanning 530005, China it reduces transportation costs and makes the harvest Full list of author information is available at the end of the article process quicker and more accessible [7, 8]. In many © The Author(s) 2021. This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http:// creat iveco mmons. org/ licen ses/ by/4. 0/. The Creative Commons Public Domain Dedication waiver (http:// creat iveco mmons. org/ publi cdoma in/ zero/1. 0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Peng et al. Biotechnol Biofuels (2021) 14:152 Page 2 of 10 countries, the harvested cane is kept in the feld for 30 °C. Te pH of all the bagasse reduced signifcantly 3–5 days due to the fawed feld transport system and in the frst 12 h (one-way ANOVA, p < 0.001) and then 1–3 days in the factory storage under undesirable con- maintained at around 3.6–3.8 (Fig. 1). ditions [2, 5]. Sucrose inversions in the deterioration of harvested cane result from the chemical (acid), enzymic Diversity of fungal communities inversion, and microbial activity. In the frst 14 h of cane For determining the fungi prevailing in biodegrading juice deterioration, 93.0% of sucrose losses are caused sugarcane, microbial community DNA was extracted and by microbial, 5.7% by enzymic, and 1.3% by chemical amplifed using the ITS2 primer pair (Additional fle 1: changes (acid degradation) [3]. Microorganism plays a Fig. S3). Subsequently, the amplicons were sequenced signifcant role in biodegradation and changes of host on the Illumina MiSeq platform. A total of 962,640 chemical characteristics [9, 10]. Te high sugar concen- reads were recovered from all samples after quality fl- tration within the mature internodes provides a favora- tering (Additional fle 1: Tables S1 and S2), representing ble environment for microbial thriving, which enters the 31 fungal Operational Taxonomic Units (OTUs) at 97% harvested stalk through wounds or cut ends [6]. Also, sequence similarity. Te rarefaction curves confrmed leaf sheaths and growth cracks provide excellent sites for that all the samples reached the plateau phase (Addi- microbial growth. Over 400 species of bacteria and fungi tional fle 1: Fig. S1). Te richness and diversity of fun- are associated with sugarcane products [11]. After mill- gal OTUs rose in the frst 12 h in all the samples. Te ing, Penicillium, Lactobacillus, Leuconostoc, and yeast fungal richness and diversity were signifcantly lower in invade the stored sugarcane [2, 12, 13]. Tese acid-pro- the bagasse stored at 40 °C for 60 h than those stored at ducing microorganisms cause deterioration, decreasing 30 °C (p ≤ 0.05) (Fig. 2). Principal component analysis sucrose content, juice purity, and pH, especially under was used for the OUT data obtained from the 12 treat- anaerobic conditions such as mud-coated canes and the ments and three pre-treatments (CK) after standardi- cane stored in large piles with poor ventilation [5, 13]. zation as described in the Methods. Te frst principal Te glucose and fructose are converted to organic acids component accounted for 45% of the total variance in the and mannitol by the enzymes secreted by these microor- data set, while the second principal component explained ganisms. Besides these external microbes, the endophytic 22%. Bagasse stored at 30 °C and 40 °C were quite difer- microbial genera viz., Acetobacter, Enterobacter, Pseu- ent from the pretreated bagasse (CK) (Fig. 3). Te storage domonas, Aeromonas, Vibrio, Bacillus, and lactic acid temperature alone explained 34.7% of the microbial com- group are also responsible for the deterioration of juice munity variation (PERMANOVA, p = 0.020), while the quality during staling [13, 14]. storage duration explained 73.7% of the variation (PER- It is crucial to identify the key players in sugarcane MANOVA, p < 0.001). deterioration and improve early detection strategies Only Ascomycota was identifed at the phylum level. of degradation-causing microbes. Te sucrose-related Four classes were identifed at the class level, including dynamics of fungi in stored sugarcane bagasse remain Saccharomycetes, Dothideomycetes, Sordariomycetes, and unexplored. Tereby, the fungal community variations Eurotiomycetes, of which Saccharomycetes accounted for in the stored bagasse were analyzed for assessing the 99.7%. Five orders were identifed, including Saccharomy- core fungi and specifc biodegradation biomarkers using cetales, Pleosporales, Hypocreales, Chaetothyriales, and high-throughput sequencing. Moreover, the study also Eurotiales, of which Saccharomycetales alone accounted explored the impact of diferent cane storage durations for 99.7%. At the family level, ten families were identifed, and temperatures on sugarcane deterioration and dis- of which Saccharomycetaceae accounted for 64.1%, fol- sected these parameters associated with the fungal rich- lowed by Phafomycetaceae (35.3%). Further, at the genus ness and diversity. level, a total of 14 fungal genera were identifed. Saccha- romyces, Torulaspora, Hanseniaspora, and Curvularia Results were exclusively present in the bagasse stored at 40 °C, Sucrose and pH while Kazachstania, Zygosaccharomyces, and Hansenias- In the frst 12 h, the steepest decline was observed in the pora were solely identifed in bagasse stored at 30 °C. Te bagasse stored at 30 °C. Te sucrose reduced by 53.9% dominant genus in CK bagasse was Wickerhamomyces within the frst 12 h and then completely decomposed (92%). during the initial 36 h for all the treated bagasse. Con- When the bagasses were stored at 30 °C, Kazach- trary to sucrose, the glucose and fructose of the bagasse stania gradually replaced Wickerhamomyces as the increased in the frst 12 h and then fell to zero by 60 h most abundant fungus (60% at 12 h and 80% at 60 h). (Fig. 1b, c). However, the glucose and fructose increased However, the bagasses stored at 40 °C for 12 h had two in the bagasse stored at 40 °C was higher than those at highly abundant genera of Saccharomyces (50%) and Peng et al. Biotechnol Biofuels (2021) 14:152 Page 3 of 10 Fig. 1 Properties of sugarcane stem samples. Sucrose (A), glucose (B), fructose (C), and pH (D) profles in the stem powder recorded during the storage period.
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