Constructing Micro-Landscapes: Management and Selection Practices on Microbial Communities in a Traditional Fermented Beverage

Introduction

Throughout history, human societies have developed knowledge and techniques to use a plethora of species of plants, animals, fungi and other organisms from different ecosystems to satisfy nutritional needs (Campbell-Platt, 1994; Tamang et al., 2016, 2020, 2021). Interactions between people and nature commonly include a high diversity of management practices through which people adequate organisms and other components of ecosystems to secure their livelihoods; these practices are context-dependent on local conditions, outstandingly human culture and environment (Jones et al., 1997; Odling-Smee et al., 2003; Anderson, 2005). Traditional or local knowledge commonly includes complex bodies of information on the ecological context, relationships and behavior of the elements used as food, extensive repertoires of preparation procedures, as well as about their relationships with customs, taboos, rituals, and other cultural aspects (Nabhan, 2010; Tamang, 2010; Ratcliffe et al., 2019). All these biocultural facets can be visualized through the diversity of food products and practices related to it, and provide basic notions about what is edible, where and when edible elements are available, the way these should be harvested, and how they can be improved by cooking, roasting, fermenting, or making it harmless (Lévi-Strauss, 2012; Ratcliffe et al., 2019; Tamang et al., 2020, 2021; Tsafrakidou et al., 2020; Fernández-Llamazares et al., 2021; Gadaga et al., 2021; Kennedy et al., 2021).

Fermentation practices are part of the local knowledge and food systems, directed to procure and improve human health and wellbeing, but fermented products have changed the human food supply worldwide (Harris et al., 1989; Kuhnlein and Receveur, 1996; Steinkraus, 1996; Harris, 1998; Quave and Pieroni, 2014; Svanberg, 2015; Sõukand et al., 2015; Flachs and Orkin, 2019; He et al., 2019). Fermentation can contribute to construct sustainable food systems, diversify food production, and procure safety, security and sovereignty in human communities around the world (Johns and Sthapit, 2004; Marshall and Mejia, 2011; Ojeda-Linares et al., 2021). It allows preserving and improving nutritional value of food and conferring desirable properties to the final products such as textures and sensorial properties, which are completely unlike to those of the starting materials (Smid and Hugenholtz, 2010; Smid and Kleerebezem, 2014). The microbial communities of bacteria, yeasts, and molds play a key role determining the quality of the fermented products, influencing their acidity, flavor, texture, nutritional value and other health benefits (Forssten et al., 2011; Todorov and Holzapfel, 2015; Gutiérrez-Uribe et al., 2017; El Sheikha and Hu, 2020). Changes in the microbial composition may be caused by variation in environmental factors, thus organoleptic and physicochemical characteristics of a fermented product could be modified and driven by managing fermentation environments through human practices (Escalante et al., 2016; Rebollar et al., 2017). The persons that perform and drive changes and follow the fermentation process in traditional contexts are recognized as traditional fermentation managers (Nabhan, 2010; Flachs and Orkin, 2019; Ojeda-Linares et al., 2020).

A common practice used to produce traditional ferments is the “spontaneous” fermentation, which involves microorganisms occurring in a local environment and is influenced by temperature, substrate type, techniques and tools employed, and other cultural factors that shape the composition and dynamics of the microbiota (De Vuyst and Vancanneyt, 2007; Vogelmann et al., 2009; Chaves-López et al., 2020). Due to the influence of all these factors, this type of fermentation is commonly assumed to be unpredictable, producing outcomes of inconsistent attributes; local people commonly have knowledge about how environmental and technological factors may influence the product and carry out practices to manage them, looking for decreasing the unpredictability of the resulting product. The other general practice is the use of starter cultures, which are characteristic for numerous fermented products around the world. Inoculation refreshment favors a periodically stable microbial community which provides an easy way to achieve optimal fermentations and desirable products (De Vuyst and Vancanneyt, 2007; De Vuyst et al., 2009; Brandt, 2014; Harth et al., 2016; Mukisa et al., 2017). Therefore, it is thought that this type of practice is associated with a set of selective forces favoring a specific community of microorganisms, guiding the dynamics and structure of the microbiota through the fermentation process (Vogelmann et al., 2009; Vogelmann and Hertel, 2011; Gibbons and Rinker, 2015; Liu et al., 2021).

The influence of human management over composition, structure and dynamics of microbial communities has been insufficiently analyzed, even when humans historically have developed numerous management techniques to direct, diversify and innovate the quality or to prevent the spoilage of fermented products around the world (Tamang and Fleet, 2009; Tamang et al., 2016). Ethnozymological studies have documented a wide range of activities that producers perform to adequate fermented products to their purposes; for instance, boiling the substrates, adding salt, plant, or animal products with antiseptic or flavoring roles are common practices (Quave and Pieroni, 2014; Hong et al., 2015; Sõukand et al., 2015; Pieroni et al., 2017; Álvarez-Ríos et al., 2020; Ojeda-Linares et al., 2021). Documenting the known-how of the management over the microbial communities in fermented products has high importance to understand the implications of human practices on the structure and dynamics of microbial communities during fermentation and to recover old human experience for innovation. In addition, this information provides elements to analyze possible processes of domestication at species and/or community levels.

Management includes a broad spectrum of practices that favor phenotypic attributes of organisms like size, flavors, colors, nutritional values, attributes to satisfy customs, rituals, ornamental, and other cultural purposes (Anderson, 2005; Casas et al., 2007). Through time, management has determined differences between wild and managed populations, the latter having higher frequencies of human-favored phenotypes. Such processes have been especially assessed in plant and animal populations where specific visible phenotypes are favored (Casas et al., 2007; Blancas et al., 2010). At ecosystem level, management practices may be directed to change species richness, diversity, and structure of communities and this is also an expression of domestication, the landscape domestication (Casas et al., 1997; Smith, 2007; Albuquerque et al., 2019; Clement et al., 2020, 2021; Franco-Moraes et al., 2021). But, although the processes involved in ecosystem management are common and widespread throughout the world, these have been less studied than domestication at species populations level and even fewer are studies documenting management and domestication at micro-landscape level.

In this study we explored the general hypothesis that the composition and structure of the microbiota involved in fermentation would differ according to management practices. We expected to find a higher microbial diversity in techniques involving spontaneous fermentation than in those using inoculums, which would be favoring reduced consortiums of microorganisms due to continuous human selection. Such differences would also influence the dynamics of change through the fermentation of communities with higher and lower diversity toward less and more predictable products, respectively. Characterizing and analyzing the type and extent of change of microbial communities according to management practices are conceptually relevant to construct and test hypotheses about how these processes and techniques lead to domestication of microorganism consortiums and, probably, of specific lineages. Also, to design innovative strategies to improve food quality. Understanding how certain management practices do help to predict how diversity, composition, and richness of microbiota can be and change, would support principles of selection and management programs of microbial communities to obtain desirable products.

Such hypothesis has been narrowly explored, particularly because testing it requires methods and study systems able to compare and measure across confidently. A traditional fermented product prepared with the same substrate and different management practices represents an optimal study system for such purpose, while using High Throughput Sequencing (HTS) techniques allow detecting or rejecting associations between microbial composition and management practices. Currently, HTS allow glimpsing the composition and structure of microbial communities in different ecosystems (Metzker, 2010; Caporaso et al., 2011) and fermenting landscapes are not the exception (Foligné and Pot, 2013; De Filippis et al., 2017; Sha et al., 2018; Astudillo-Melgar et al., 2019).

To address our hypothesis, we selected the traditional fermented beverage called colonche. Colonche is a group of traditional Mexican beverages prepared since pre-Columbian times by the fermentation of fruits of several cactus species, including several species of Opuntia prickly pears and columnar cacti (Ojeda-Linares et al., 2020). We conducted our study in the Meridional Central Plateau region of Mexico, where the main substrate for colonche production is Opuntia streptacantha fruit. For its production, prickly pear fruits are gathered in wild and cultivated populations and stored in plastic trays almost every day from August to October, when fruits are available. Local people carry out different fermentation practices, based on spontaneous or inoculated procedures. To produce colonche through spontaneous fermentation, they harvest and peel the Opuntia fruits in situ, and then place them inside a clay pot where fermentation occurs for about 12 h. In this area the colonche production is mainly performed by old men (60 ± 5 years old). The inoculated fermentation is performed by firstly boiling the fruits to concentrate their juice; then, the producers add the starter cultures from previous batches and store the fermenting juice in plastic containers for 4 h (Ojeda-Linares et al., 2020). The production of inoculated colonche in the area is mainly performed by young women (32 ± 4 years old), and the production represents a recent recovery of this beverage by the younglings. Therefore, an analysis of the microbiota associated with this fermented beverage prepared with the same substrate under different fermentation practices is possible and would allow documenting how management over the fermentation process influences the microbial communities.

Nowadays, there is a worrying erosion of local food systems, causing the disappearance of traditional food products worldwide (Pingali, 2007; Turner and Turner, 2007; Johns et al., 2013; Albert et al., 2015; Hernández-Santana and Narchi, 2018; Akinola et al., 2020). Fermented products have been poorly considered in the analysis of erosion of local food systems, even when some of them have almost disappeared. Nonetheless, a renewed interest in their production has motivated studies and actions to guarantee its permanence (Madej et al., 2014; Svanberg, 2015; Cano and Suárez, 2020; Ojeda-Linares et al., 2020, 2021). In México, it has been recorded the loss of some traditional fermented beverages, even though the main substrates are available in the nearby, but the transmission of knowledge has been lost (Ojeda-Linares et al., 2021). The vanishing of fermented products not only favors disappearing fragments of foodscapes, but also the traditional ecological knowledge over fermentation practices, and therefore the efforts that humans have historically engineered to shape microbial communities and the evolutionary processes involved in making unique products.

This study aims to describe the microbial community of colonche under different management practices and highlights the relevance of traditional knowledge to construct the micro-landscapes and, in general, to preserve unique products that are part of a local food systems. We aspire to contribute to a deeper understanding of the processes that can be involved in the selection and domestication of microbial consortia and specific lineages of the microbiota. We also aspire to contribute to the conservation of traditional knowledge over fermentation practices and the establishment of a microbial panel helpful to determine the geographical origin of the product and supports the relevance and the way of its conservation.

Materials and Methods

Study Area and Sampling

We studied colonche samples prepared by the fermentation of O. streptacantha fruits. We collected nine samples from spontaneous fermentations in the village of Laguna de Guadalupe (LG) in the state of Guanajuato, México from three different producers that performs similar practices. Also, nine samples of inoculated colonche produced by three producers in Mexquitic de Carmona (MC) in the neighboring state of San Luis Potosi (Figures 1A,E). We in addition collected samples of residuals from two clay pots one day before producers began spontaneous colonche fermentation. These clay pots have been used for almost 80 years for colonche production and are stored indoors when fruits of O. streptacantha are not available. Before the fermentation starts, the producers clean them only with water (no soap is added since according to people it changes the flavor of the product; Figure 1B). In addition, we collected and analyzed two samples of the inoculum, which were saved from the last production season, stored in a fridge and ready to use in the following batches (Figure 1C) and two samples of the cooked cactus prickly pear fruit juice before fermentation in the inoculated treatment (Figure 1D). The cooked samples represent a treatment that producers of the locality of Mexquitic performed because it is presumed to give a longer shelf life to colonche, since it can be stored in this way before the inoculum is added.

FIGURE 1

Figure 1. Sampling sites and colonche samples (A1) the locality of Laguna de Guadalupe in Guanajuato state; (A2), Mexquitic de Carmona in San Luis Potosí. (B) Claypots where spontaneous fermentation occurs; (C) Inoculum stored from the last season; (D) Cooked and boiled Cactus prickly pear fruits where sugars are concentrated; (E) Inoculated samples ready to sell in the local markets.

DNA Extraction and Sequencing

Genomic DNA was extracted for all the samples with the ZR Soil Microbe DNA MiniPrep kit (Zymo Research) following the manufacturer’s protocol. DNA was quantified using Qubit Fluorometric Quantitation (Thermo Fisher Scientific) and its quality was assessed on a 1% agarose gel. The obtained high-quality DNA samples were stored at −20°C util the library preparation. The libraries and targeted metagenomic sequencing were performed at ZymmoBIOMICS Service (Irvine, CA). Libraries of 16S rDNA and ITS amplicons were sequenced on the Illumina^® MiSeq™ platform 2 × 300 bp paired end. For bacteria, the V3-V4 regions of the 16S rRNA were amplified as has been reported in previous works (Caporaso et al., 2011; Li and Yue, 2016). For fungi, the internal transcribed spacer (ITS) was amplified using the ITS2 primers (Yao et al., 2010; Badotti et al., 2017; Baldrian et al., 2021).

Microbiome Analysis in the Colonche Samples

The 16S rRNA and ITS amplicon sequences were processed using QIIME 2™ (Caporaso et al., 2010; Bolyen et al., 2019), version qiime2-2018.8. For all data, the DADA2 (Callahan et al., 2016) pipeline was used for quality filtering, removal of chimeric sequences, merge paired end reads and generate a table of amplicon sequence variants of each dataset (ASVs, Callahan et al., 2017). To eliminate the bases corresponding to the primers, the first 16 bases of the forward reads and 24 bases of the reverse reads of the 16S rRNA sequences were trimmed. From the ITS sequences, 22 and 24 bases of forward and reverse reads were clipped, respectively. Furthermore, to remove low-quality regions of the sequences, each read was clipped to some position where the quality decreases and was determined with the interactive quality plots of QIIME 2™ (Bolyen et al., 2019). The 16S rRNA sequences were truncated to 315 bases for forward reads and 250 bases for reverse reads, and the ITS sequences were truncated to 310 bases and 215 bases for forward and reverse reads, respectively.

Taxonomy was assigned to the representative unique sequences from each ASVs based on the Naïve Bayes classifier (Bokulich et al., 2018) and annotated according to the Greengenes 13_8 database (DeSantis et al., 2006); for the 16S rRNA data and from the ITS data the UNITE database v8.0 (Nilsson et al., 2019) was used. For each dataset, the ASVs represented by less than 10 sequences were removed in all samples, and the ASVs that were classified as plant chloroplast, mitochondria, archaea, unassigned sequences, or only assigned to phylum level were also eliminated. For diversity and statistical analysis, the ASVs tables of bacteria and fungi were normalized by their relative abundance (Fitzpatrick et al., 2018; Solís-García et al., 2021).

Diversity and Statistical Data Analysis

Alpha diversity was evaluated with the Hill numbers (^qD), where the order q determines the sensitivity of the measure to the relative abundance (Chao and Chiu, 2016). ⁰D is equivalent to the richness; the measure ¹D counts the ASVs proportionally to their abundances and corresponds to the effective numbers of common ASVs; the measure for ²D considers the most abundant ASVs and can be interpreted as the effective number of dominant ASVs (Chao et al., 2014; Montes-Carreto et al., 2021). The comparisons of the diversity measures among colonche management practices were made under the same sample coverage and the no overlap in the 95% CI values indicates significant differences (Cumming et al., 2007). Sample coverage values, ^qD, and their confidence intervals were calculated with the iNEXT R package 3.5.3 (Hsieh et al., 2016), using as an endpoint the maximum number of sequences in each treatment.

For beta diversity analyses, each phylogenetic tree was constructed with the ASVs of bacteria or fungi of the inoculated and spontaneous colonche management practices. The sequences alignment was made with MAFFT, the trees were inferred with FastTree and then rooted at its midpoint. The ASVs tables of bacteria and fungi log2-transformed and the dissimilarity matrices of the Unifrac weighted and unweighted distances were calculated with the phyloseq (McMurdie and Holmes, 2013) and vegan packages (Oksanen et al., 2013). The phylogenetic dissimilarities of the bacterial and fungal communities were represented with the ordination method of non-metric multidimensional scaling (NMDS) based on the Unifrac weighted and unweighted distances (Lozupone et al., 2011). To compare the structure of each community of the inoculated and spontaneous colonche management practices a permutational multivariate analysis of variance (PERMANOVA) was computed using the vegan package with 999 permutations.

Significant differences in the relative abundance of each taxon between the inoculated and spontaneous colonche management practices were evaluated through the Mann-Whitney-Wilcoxon test with an FDR correction in R v.3.5.2 software, considering as a significant values P < 0.05. The shared bacteria and fungi ASVs among both treatments were plotted as a Venn diagram with the VennDiagram package (Chen and Boutros, 2011).

Results

Preprocessing and Taxonomic Classification

To visualize the changes in the bacterial communities between fermentation management practices we obtained pair-end sequencing of the V3-V4 region of the 16SrRNA leads to a total of 2,398,545 reads, with an average of 28,769.79 (± 33,516.46) reads per sampling, then, after filtering the ASVs table, a total of 701 in all 16S samples, belonging to 173 bacterial genera (Supplementary Table 1). For fungal communities by ITS sequence, a total of 1,505,383 pair-end were obtained with an average of 62,724.291 (± 23,303.49) reads for all the sampling which composed a total of 203 ASVs; then, after filtering the table with 0.01% of relative abundance, 201 ASVs were obtained, belonging to 187 yeast genera (Supplementary Table 1). The bacterial and fungal communities of each colonche management practices had a sample coverage of 100% suggesting that the most of the ASVs were captured (Supplementary Figure 1A). Also, rarefaction curves for all the samples reached the plateau indicating that the sequencing depth was sufficient to cover most of the bacterial and fungal diversity in each colonche management practices (Supplementary Figure 1B).

Colonche Microbiome Is Partially Consistent With the Management Hypothesis

To analyze our hypothesis, the alpha diversity was estimated using the Hill numbers (^qD). For the ASVs of the bacterial community (Supplementary Table 2), the clay pots samples showed a higher richness (⁰D = 543 ± 0.121), followed by the spontaneous samples (⁰D = 136 ± 0.433), the inoculated samples (⁰D = 128 ± 0.929), the cooked samples (⁰D = 113.00 ± 3.485), and being the inoculum samples (⁰D = 47 ± 0.163) the ones with the lowest richness (Figure 2A). Also, the clay pot samples were the most diverse (¹D = 131.575 ± 1.412, ²D = 38.087 ± 1.212) compared with the other colonche management practices (Figures 2B,C and Supplementary Table 2). The diversity values of the effective number of common and dominant ASVs were significantly higher in the inoculated samples (¹D = 18.277 ± 0.929, ²D = 11.507 ± 0.04) contrarily to the spontaneous samples (¹D = 11.081 ± 0.049, ²D = 4.33 ± 0.019; Figures 2B,C). Thus, there is a reduction in richness from spontaneous to inoculated fermentation practices in the colonche microbiome, which is consistent with our hypothesis. The richness of the ASVs of the fungal community (Figure 2D and Supplementary Table 2) showed a different pattern, the clay pots also display the highest values (⁰D = 159 ± 0.151), followed by the inoculated samples (⁰D = 32 ± 0.539), then the cooked samples (⁰D = 31 ± 0.458), the spontaneous samples (⁰D = 19 ± 0.917), and finally the inoculum with the less richness (⁰D = 3 ± 0.151). Diversity of clay pots samples (¹D = 28.873 ± 0.214, ²D = 14.787 ± 0.145) was higher than that of the other colonche management practices (Figures 2E,F). In contrast, diversity of common and dominant fungal ASVs was significantly higher in the spontaneous samples (¹D = 2.667 ± 0.004, ²D = 2.442 ± 0.004) than in the inoculated samples (¹D = 1.826 ± 0.007, ²D = 1.346 ± 0.004; Figures 2E,F).

FIGURE 2

Figure 2. Comparison of the richness and alpha diversity of the bacterial (A–C) and fungal communities (D–F) between the different colonche management practices estimated with the Hill numbers (^qD). Interval plots of richness (A,D), effective number of common amplicon sequence variants (ASVs) (B,E), and effective number of dominant ASVs.

Colonche Microbial Differences Between Spontaneous and Inoculated Fermentation Practices

To characterize the differences between spontaneous and inoculated colonche microbiome, the beta diversity of bacterial and fungal communities was represented with a NMDS using weighted and unweighted Unifrac distances (Figure 3 and Supplementary Figure 2). Although phylogenetic dissimilarities between the bacterial groups in spontaneous and inoculated fermentations by the unweighted Unifrac distance allow visualizing the splitting of both bacterial communities (p < 0.036), there is an inoculated sample that is closer to the spontaneous samples, and the spontaneous fermented samples are more disperse and less clustered (Figure 3A and Supplementary Table 3). The weighted Unifrac distances partially allow discriminating fungal community (p < 0.047), it can be seen that the spontaneous bacterial communities are clustered, while the inoculated samples are more variable and there are samples that overlap with the spontaneous treatment (Figure 3B and Supplementary Table 4). Both results are supported by PERMANOVA analysis (999 permutations). Summarizing, the overlap in microbial communities for both types of fermentation practices might reflect a common shared composition of microorganisms occurring in the Opuntia streptacantha substrate. The variation in the spontaneous bacterial community is consistent with the data of alpha diversity, while for fungal communities there are less differences among treatments, which might reflect the high abundance and dominance of Saccharomyces genus, as referred to for alpha diversity (Figure 2B).

FIGURE 3

Figure 3. Non-metric multidimensional scaling (NMDS) plots-based (A) on UniFrac weighted distance of the bacterial community structure; (B) an Unifrac weighted distances of the fungal community structure associated with inoculated and spontaneous fermentation practices in the colonche production.

Colonche Microbial Genus Composition in the Different Fermentation Practices

The Microbial Community in Spontaneous Fermentation: Clay Pots and Spontaneous Colonche

Besides different diversity levels, we found that clay pots have a high richness in the composition of bacteria and fungi at the genus level (Figure 2). Among the most abundant bacteria genera occurring in the clay pots are: Arthrobacter (14.92%), Elstera (10.12%), Alkanindiges (7.72%), Massilia (6.92%), Pseudomonas (5.18%), Nocardioides (1.79%), Roseomonas (1.62%), Rhizobium (1.40%), Blastococcus (1.39%), Achromobacter (1.20%), Brevundimonas (1.15%). While for fungal community, Penicillium (38.15%), Cladosporium (9.70%), Didymella (9.60%), Wickerhamomyces (8.90%), Naganishia, (7.86%), Alternaria (6.42%), Rhodotorula (4.06%), Fusarium (3.02%), Saitozyma (1.62%), Aureobasidium (1.38%), Vishniacozyma (1.14%), Cystofilobasidium (1.01%) and although Saccharomyces (0.42%) ends up as the most dominant yeast in the spontaneous fermentation, its abundance is lower in the clay pots (Figure 4).

FIGURE 4

Figure 4. Composition of the (A) Bacterial Genera composition of the community associated with the management practices and colonche production stages and, (B) the fungal Genera composition. Low abundance taxonomic groups (relative abundance < 1%) were reported as others. NA mean not assigned. The asterisk indicates significant differences in taxa relative abundance between management practices.

At the end of the spontaneous fermentation process, 10 fungal ASVs (Aureobasidium, Candida, Cladosporium, Pichia, Saccharomyces, Torulaspora, Rhodotorula, Wickerhamomyces, one unidentified taxon and one not assigned fungal) are shared within the clay pots. This group is mainly involved in the final stages of the fermentation process of the spontaneous fermentation. Four groups are exclusive of the spontaneous fermented colonche (Dekkera, Kazachstania, Kluyveromyces and Knufia) and 45 are unique for clay pots. This behavior is similar in the bacterial community, in which 6 genera (Massilia, Elizabethkingia, Clostridium, Bacillus, Alkanindiges and one not assigned taxon) are shared with the spontaneous final product and the clay pots. For instance, 12 genera (Weissella, Tanticharoenia, Tatumella, Streptococcus, Rheinheimera, Pediococcus, Lactococcus, Lactobacillus, Gluconacetobacter, Faecalibacterium, Dorea and Aeromonas) are present in the final product of spontaneous fermentation, being particularly remarkable Lactobacillus and Leuconostoc, which are present in higher abundance (Figure 4). Finally, 71 ASVs are exclusive of the microbiota communities of the clay pots.

The Microbial Community in the Inoculated Fermentation: Inoculums, Cooked and Inoculated Colonche

It can be visualized that the inoculums are the samples with the lowest richness of bacteria and yeasts; for instance, we identified only 7 bacteria and 2 yeast genera, mainly dominated by multiple taxa of Lactic Acid Bacteria (LAB) as: Lactobacillus (24.60%), Leuconostoc (10.34%), Alkanindiges (8.65%), Pediococus (6.92%), while yeasts are dominated by Saccharomyces (99.9%) and Kazachstania (0.01%). Surprisingly, there were a higher number of ASVs for the cooked samples with 32 bacteria genera (Supplementary Table 5) and 21 yeasts, contrasting with the final product of the inoculated fermentation, which had fewer ASVs (Supplementary Table 6).

As mentioned above, in the inoculated fermentation process all microbial ASVs of the inoculums are shared with the inoculated final product. Also, Alkanindiges, Clostridium Corynebacterium, Gluconacetobacter, Lactobacillus, Leuconostoc, Massilia, Pediococcus, Sphingomonas, Staphylococcus, Weissella and one not assigned taxon are shared between the cooked and the inoculated samples. Dorea and Elstera are the only two exclusive genera of the inoculated samples and 18 genera (Actinomycetospora, Actinotelluria, Albidovulum, Arthrobacter, Blastococcus, Dietzia, Gaiella, Helcobacillus, Micrococcus, Microlunatus, Nocardioides, Oceaniovalibus, Ochrobactrum, Roseomonas, Solirubrobacter, Sporosarcina, Streptomyces and Tanticharoenia) are exclusive of the cooked samples.

For the fungal community we registered 9 genera being commonly shared between the cooked treatment and inoculated samples (Candida, Cladosporium, Dipodascus, Hanseniaspora, Kazachstania, Kluyveromyces, Saccharomyces, Torulaspora and one unidentified taxon). The genera Alternaria, Arthrinium, Cryptococcus, Didymella, Filobasidium, Fusarium, Mucor, Naganishia, Rhodotorula and Starmerella are exclusive of cooked samples and only Aureobasidium, Dekkera, Issatchenkia and Pichia are unique for the final product of inoculated fermentation.

The Microbial Composition Between Spontaneous and Inoculated Fermentations

For bacterial communities we found that 12 ASVs are shared among the fermentation practices, like Lactobacillus (p < 1e-1), Alkanindiges, Clostridium, Dorea, Faecalibacterium, Gluconacetobacter, Lactococcus, Leuconostoc (p < 1e-1), Pediococcus (p < 1e-1), Tatumella, Tanticharoenia, and Weisella (p < 1e-1). For instance, 6 genera are exclusive to spontaneous treatment like Aeromonas, Bacillus, Elizabethkingia, Massilia, Rheinheimera and Streptococcus and 4 are exclusive of the inoculated samples (Staphylococcus, Sphingomona, Corynebacterium, Elstera) (Figure 5A). In the fungal communities, we identified 11 genera shared among samples under different fermentation practices: Aureobasidium, Candida, Cladosporium, Dekkera (p < 1e-1), Hanseniaspora, Kazachstania (p < 1e-6), Kluyveromyces, Pichia, Saccharomyces, Torulaspora and other unidentified taxa. The inoculated samples displayed 4 exclusive ASVs (Wickerhamiella, Issatchenkia, Dipodascus and Clavispora), while the spontaneous fermentation samples registered 3 unique ASVs (Wickerhamomyces, Knufia and one not assigned genus) (Figure 5B).

FIGURE 5

Figure 5. Venn diagrams of the number of unique and shared amplicon sequence variants (ASVs) of the (A) bacterial and (B) fungal community associated with the fermentation practices of colonche samples inoculated (red) and spontaneous (purple).

Discussion

Differences Between Spontaneous vs. Inoculated Fermentations

Our results confirm that spontaneous and inoculated fermentation practices significantly differ in the composition of microbial assemblages and the relative abundance of bacterial and fungal taxa in fermenting communities. These results are in concordance with most of the literature reporting that spontaneous fermentations exhibit a higher number of microbial species than inoculated products (Tamang et al., 1988; Raspor et al., 2002; Haruta et al., 2006; Domizio et al., 2007; Alves et al., 2010; Hong et al., 2015; Anagnostopoulos et al., 2020; Lu et al., 2021). These results confirm the reduction of diversity hypothesis, as can be visualized in Figure 2, where the lowest values of diversity for both bacteria and fungi were recorded in the inoculums and the reduction at the final composition for bacterial communities occurs in the inoculated samples. Nevertheless, this relation is not unidirectional for fungi, for which we observed small differences, contrarily to what has been previously reported (Raspor et al., 2002).

Fermentation traditionally occurs spontaneously and is initiated by a diverse community of indigenous yeasts and bacteria associated to the plants, the environment, or the fermentation facilities where it is produced (Pretorius et al., 1999; Motarjemi, 2002; Bokulich et al., 2013; Bokulich and Mills, 2013; da Silva Vale et al., 2021). In different traditional fermented beverages, the yeast genera Hanseniaspora, Pichia, Metschnikowia, Candida, Torulaspora, Rhodotorula, Cryptococcus, Lachancea, Zygosaccharomyces have been recorded as the most common at the initial stages of the successional process of fermentation, while strains of Saccharomyces cerevisiae become dominant at the last stages (Krieger-Weber et al., 2020). Although successional dynamics were not assessed in our current analysis, it could be considered that the fermentative environment as the clay pots where spontaneous fermentation occurs and the cooked samples before the inoculation, displayed a higher richness at both initial stages. This information also confirms that there is a marked dominance of the genus Saccharomyces at the final stages of the fermentation, and it occurs independently if it is spontaneous or inoculated fermented colonche. This can be explained because of the Saccharomyces capacity to quickly adapt to variable environmental conditions (Legras et al., 2018).

Our results confirm that the non-Saccharomyces yeast group comprises a variety of oxidative, weakly fermentative and strongly fermentative yeasts of genera like Rhodotorula, Cryptococcus, Hanseniaspora, Candida, Pichia, Issatchenkia, Metschnikowia, Lachancea, Zygosaccharomyces, Starmerella, Torulaspora and others (Barata et al., 2012), which are found at different frequencies at the clay pots and the cooked samples. This group has low fermentation power and are sensitive to prevailing anoxic conditions and increasing ethanol levels (Martinez et al., 2013; Quirós et al., 2014; Morales et al., 2015). Depending on the fermentative capacity and metabolic activity of the individual species, non-Saccharomyces yeasts are able to maintain their viability until the middle of fermentation before starting to decline (Xufre et al., 2006; Renouf et al., 2007; Andorrà et al., 2008; Zott et al., 2008, 2010; Bagheri et al., 2015; Sha et al., 2017). Nevertheless, the current results showed the dominance of Saccharomyces over the non-Saccharomyces groups in the final products of both types of fermentations. A similar observation was reported for other fermented beverages around the world (Tamang et al., 1988; Lyu et al., 2013; Yang et al., 2016; Sha et al., 2017).

In both types of fermentation, we identified constantly the Pediococcus genus. Some species of this genus are associated with spoilage of fermented beverages, especially beers and wines (Mokoena, 2017). It has been associated with the synthesis of excessive diacetyl, exopolysaccharides, and biogenic amines, all of which have a detrimental impact on the quality of the product (Wade et al., 2019). However, recent research has supported the contention that Pediococcus spp. can grow in wines considered to be microbiologically stable. In fact, the presence of Pediococcus spp. in wines not always lead to spoilage, and new findings have suggested potential uses for Pediococcus spp. to contribute to desirable characteristics of wines under certain circumstances. As Pediococcus was one of the most common genera identified in colonche samples, further studies through High-performance liquid chromatography (HPLC) should be addressed to characterize if the high abundance is associated with the spoilage or if it brings desirable characteristics to colonche and the distinction in the aromatic profile between fermentation practices.

The presence of yeast genera like Wickerhamiella, Clavispora, Dipodascus and Issatchenkia, has been described previously in pulque fermentation (Rocha-Arriaga et al., 2020). For instance, the differences of the fungal community between the inoculated fermentation are due to the common use of pulque to improve their fermentation or the use of the same containers for pulque production. Torulaspora is one of the few microorganisms previously identified in colonche samples (Ulloa and Herrera, 1978). By the current sampling we identified its presence in clay pots and in the cooked samples, which might represent the initial stages of fermentation. However, at the end of the fermentation under both types of practices low numbers of this genus were identified, and such low population density may be due to strict anaerobic conditions and low invertase activity (Visser et al., 1990; Hanl et al., 2005), mainly promoted by Saccharomyces species.

Kluyveromyces was also found in the colonche samples, it is a genus that has been isolated from a great variety of habitats and has been described to have high metabolic diversity and a substantial degree of intraspecific polymorphism. Therefore, several different biotechnological applications have been investigated with this yeast: production of enzymes, single-cell protein, aromatic compounds, and other applications (Varela et al., 2017). However, it cannot grow under strictly anaerobic conditions and the ethanol production is almost exclusively linked to oxygen limitation (Visser et al., 1990; van Dijken et al., 1993; Bellaver et al., 2004). In this sense, the higher abundance of Kluyveromyces genus in cooked and inoculated colonche samples might be due to a low alcohol content, but further studies are still needed to address the relationship between physicochemical attributes and the presence of microbial communities.

Kazachstania genus is typically encountered in the plant substrate, for instance, it is associated with grapevines and, in a low frequency, in grape must. Although it has not yet been characterized in cactus prickly pear fruits, this yeast genus provides positive aroma attributes that should be explored further. Its low presence in the final inoculated colonche product might be due to the dominance of the Saccharomyces which display a higher abundance in this treatment. Rhodotorula is also a common basidiomycete yeast that has been reported in several dairy products, it has a weak fermentative capacity, and has also been found associated with insects as vectors (Fonseca and Inácio, 2006; Kemler et al., 2017). The presence of this basidiomycete yeast might reflect the presence of insects closer to the clay pots and the low cautions in the storage of the cooked substrate. Nevertheless, this yeast was not found at the end of fermentation under both treatments, suggesting that hygienic practices are performed or inhibited during fermentation. In general, fungi held more stable ranges of diversity indexes in most of the samples analyzed, a similar pattern previously reported in beverages like pulque (Rocha-Arriaga et al., 2020).

Multiple strains of LAB from the Lactobacillus genus were registered in this study, Lactobacillus was the most abundant genus of bacteria, found abundantly (∼ 50%) in all phases of colonche fermentation except in clay pots. LAB are found in decomposing plant material and fruits, in dairy products, fermented meat and fish, cereals, beets, pickled vegetables, sourdough, silages, fermented beverages, juices, sewage and in cavities of humans and animals (König et al., 2009; Devi et al., 2013; Liu et al., 2014; Mokoena, 2017). LAB genera include Lactobacillus, Lactococcus, Leuconostoc, Pediococcus, Streptococcus, Aerococcus, Alloiococcus, Carnobacterium, Dolosigranulum, Enterococcus, Oenococcus, Tetragenococcus, Vagococcus and Weissella (Khalid, 2011), with Lactobacillus being the largest genus, including more than 100 species that are abundant in carbohydrate-rich substances and most of them are the most common and shared among samples of colonche in both fermentations process. It has been characterized that some LAB are used as probiotics, due to their health benefits (Ljungh and Wadstrom, 2006; De Leblanc et al., 2007; Azaïs-Braesco et al., 2010; Evivie et al., 2017). Although the main aim of this work was not to identify possible probiotics of LAB genera in colonche, we suggest that further studies in this direction may contribute to improve intestinal microbiota and human health through this beverage.

Our current study identified that 12 bacterial and 11 fungal ASVs are shared between spontaneous and inoculated colonche samples. Nevertheless, only the bacterial genera Lactobacillus, Leuconostoc, and Pediococcus and the Saccharomyces yeasts were the most abundant for both fermentation practices and appear in the inoculum and in the cooked samples. We propose as a first exploratory analysis that these 4 genera might reflect the microbial core of colonche because they appear common and abundantly in all the colonche samples. These genera are common throughout the fermentation of several fermented beverages and are closely related to food quality (Zhu et al., 2020; An et al., 2021; Ban et al., 2022). Nevertheless, further analysis as functional assignation and metaproteomics under a network approach can give insights of the functional microorganism’s core and the relevance to achieve a predictable product.

The Clay Pots: Not a Starter Culture but a Practical Reservoir for Future Fermentations

The clay pots displayed some microorganism’s genera associated with pathogenic activity, as are the cases of some strains of Clostridium, Pseudomonas, and some species of the genus Pediococcus. Nevertheless, through the fermentation stages these pathogenic strains disappear, perhaps because of the multiple strains of Lactobacillus in the spontaneous fermentation process. LAB have been applied in food preservation, partly due to their antimicrobial properties and because their capability to acidify the environment, making it harmless for other bacterial groups (Cizeikiene et al., 2013; Arena et al., 2018; Singh, 2018). Bacteriocins are a group of potent antimicrobial peptides produced by some microorganisms including LAB, primarily active against closely related organisms, mostly Gram-positive bacteria to gain competitive advantage for nutrients (Parada et al., 2007; Zacharof and Lovitt, 2012; Mokoena, 2017; Timothy et al., 2021). In fermented foods, LAB display various antimicrobial activities, through production of various metabolites, including lactic acid, hydrogen peroxide, and bacteriocins. Therefore, the high presence of Lactobacillus might reflect the drastic changes in the composition from the clay pot samples through the final product, thus inhibiting the pathogens in the environment.

As mentioned above, clay pots displayed the highest richness of bacterial and fungal genera, including several non-Saccharomyces genera, some beneficial bacterial groups as LAB and some detrimental bacterial groups associated with the spoilage of the beverage. Nevertheless, some of these microorganisms contribute to subsequent microbial growth and brings a stable community, for instance, 10 fungal ASVs and 6 bacterial genera are shared between the clay pots and the spontaneous colonche. In this sense, a stable consortium as an inoculum might not be required in spontaneous fermentation due to the presence of microbial diversity in the clay pots that can promote a starter community for fermentation process. Further studies should consider including other microbial inputs, for example the cactus pear fruits that are exposed to a variety of microorganisms derived from the environment (e.g., surfaces and soil), producer’s hands, and tools that can contribute to microbial communities and the quality of colonche as has been performed with cocoa fermentation (Schwan and Wheals, 2004; Lefeber et al., 2010; Figueroa-Hernández et al., 2019; Viesser et al., 2021), in which these factors contribute to the quality of the product.

The production of spontaneous colonche is mostly performed in clay pots, nevertheless, sometimes producers store the peeled cactus prickly pear fruits in plastic containers and then the fruits are placed inside the clay pots (Ojeda-Linares et al., 2020). Although we did not characterize the microbial and the physicochemical differences between the containers, it has been recorded that the material of the fermentation containers plays a significant role changing the abundance of specific genus as Lactococcus and Pedioccous and can affect pH values favoring a quicker fermentation (Liu et al., 2019). It is possible that the presence of these genera is favored by a previous storage in plastic containers and changes in the pH values might also change the dynamic in the clay pot by acidifying the medium. Though, further analysis should be performed to characterize the effect of the containers for colonche production.

The Inoculums: Insights for Unconscious Microorganisms’ Selection

The producers of traditional fermented beverages select inoculums as a practical way to acquire an optimal fermentation capacity and their capability to give consistent quality and aroma compositions through the fermentation process. As documented before, the selection of inoculums is related to a community of bacteria and yeasts that improves the fermentation dynamics and is mainly characterized by a reduction of diversity (Alves et al., 2010; Anagnostopoulos et al., 2020; Lu et al., 2021). In the colonche production, cinaiste is the common name of the inoculum, it is stored from previous batches year after year, and our data indicate a marked dominance of S. cerevisiae strains and a higher number of reads compared with the rest of samples analyzed. The large inoculum of active S. cerevisiae cells in most cases ensures a rapid dominance of a single strain and will therefore likely reduce any impact that the natural microbiota may have if spontaneous fermentation is allowed. In addition, the inoculum shows the lowest bacterial diversity, which is consistent with a reduced richness in starter cultures, a pattern that has been previously documented for the selection of starter cultures in other traditional fermented products (Orji et al., 2003; Zorba et al., 2003; Freire et al., 2015; Fagbemigun et al., 2021; Lima et al., 2021). Our results therefore expand the documentation of the deliberate selection of microbial consortia to acquire an optimal fermented product.

Selection of microorganisms is an attempt to enhance a fermentative environment, such type of efforts to transform the environment are proposed to play an important and underappreciated role in shaping biotic communities and evolutionary processes (Jones et al., 1997; Odling-Smee et al., 2003; Anderson, 2005). In this context, the studies of management of microenvironments can make relevant contributions to analyze general processes of domestication of organisms and their environments. Morphological and physiological changes in plants and animals show evidence of domestication and provide insights of the specific human practices that produce them. Analogous changes in microorganisms are not easy to identify. In microorganisms as yeasts, features like the overexpression of metabolic routes like maltotriose and lactate, the loss of sexual reproduction and the decreasing survival in nature, have been considered significant traits to analyze domestication (Gibbons and Rinker, 2015; Gallone et al., 2016; Gibbons, 2019), but there is still a long way to explore in this direction. However, the characterization of the practices performed to produce colonche, particularly the selection of inoculums and their specific consortia, provide a signature of deliberate human management and shaping of the fermenting microenvironments.

Summarizing, our results confirm that the choice of fermentation practice and management practices as cooking the fruits or storing batches year after year influence the composition, structure, and dynamics of microbiota communities in the different stages of colonche fermentation. Coexistence of the different fermentation practices and management techniques favors the context to maintain and diversify microbial communities involved in the colonche production. As well, through the carefully reproduction of inoculums, producers promote and direct selection over microbial communities to guide the process of fermentation. The clay pots are important reservoirs of diversity, but they are not commonly considered relevant in fermentation studies. Although the most dominant bacterial and fungal ASVs were not dominant in the clay pot, its presence might highlight the importance at the beginning of the fermentation and the practices performed to clean it are also relevant to maintain the microbial community. Finally, characterizing the management practices that the producers perform to obtain specific traditional products gives insights about the knowledge that humans have to reshape biotic communities and micro-landscapes to obtain a quality product at the end of both fermentation types. Thus, it is relevant to conserve these techniques of micro-biocultural heritage, ensure its maintenance and, in some contexts, recover it in the context of the foodscape diversity (Mintz and Du Bois, 2002; Alexiades, 2003, 2009; Marshall and Mejia, 2011; Rocha et al., 2015).

Conclusion

The characterization of the microbial communities related to the production of a traditional fermented beverage prepared with fruits of O. streptacantha under spontaneous and inoculated fermentation practices, confirmed that the fermentation practices affect the species richness, diversity, and the community structure through spontaneous and inoculated fermentation practices. However, differences are slightly significant for the final products for fungal and bacterial communities, which might be the result of the increasing relative abundance of LAB and the outstanding abundance of Saccharomyces genus in final products of both fermentation types. The current information corroborates that there is a continuous selection on microbial communities through the elaboration and management of inoculums. This practice reduces the microbial community and, in the case studied, traditional fermenters select mostly LAB and Saccharomyces genera to begin their new batches of colonche year after year. Diverse microorganisms live in the container where fermentation occurs, nevertheless, trough the fermentation dynamics the diversity changes, and a stable community is reached. Although the current research was not directed to assess the differences in the colonche quality, the microbial composition at the end of the fermentation and the demand of the consumers for this product supports that both types of fermentation practices yield a good product. However, further analysis as the characterization of microbial functionalities and the physicochemical attributes might help to improve the fermentation practices. Altogether, these results provide the potential of the traditional knowledge and management over microorganisms to produce fermented beverages, thus, the importance to maintain these products, the practices and the diversity associated over the fermentation process. These results are relevant to ensure food security and safety in localities where food availability is constrained.

Data Availability Statement

The datasets presented in this study can be found in online repositories. The names of the repository/repositories and accession number(s) can be found below: https://www.ncbi.nlm.nih.gov/, PRJNA781103.

Author Contributions

CO-L conceived, designed, conducted, collected data, and wrote the manuscript. IS-G contributed to analyze the data, constructed figures, and drafted the manuscript. AC conceived, designed, advised, funded, drafted, and reviewed all versions of the manuscript. All authors contributed to the article and approved the submitted version.

Funding

The research received financial support from the Programa de Apoyo a Proyectos de Investigación e Innovación Tecnológica, DGAPA, UNAM (IN206217 and IN206520), CONACYT (A1-S-14306).

Conflict of Interest

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Publisher’s Note

All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.

Acknowledgments

We thank the Posgrado en Ciencias Biológicas, UNAM and the Consejo Nacional de Ciencia y Tecnología CONACYT for supporting studies of Linares César. The Programa de Apoyo a Proyectos de Investigación e Innovación Tecnológica (IN206217 and IN206520), CONACYT (A1-S-14306) for financial support of the research. We also acknowledge the support of LANASE-UNAM and the following projects 2018-LN293701, 2019-LN299033, 2020-LN314852, 2021-LN31581 for the access to sequencing facilities. We especially thank people from the Altiplano region for their hospitality, generosity, and participation in the study. Most importantly for colonche preservation and sharing. Likewise, we recognize the heaviest labor to the colonche fest organizers to diffuse their cultural heritage.

Supplementary Material

The Supplementary Material for this article can be found online at: https://www.frontiersin.org/articles/10.3389/fevo.2022.821268/full#supplementary-material

Supplementary Figure 1 | Rarefaction curves of the sample coverage for (A) bacterial and, (B) fungal community. Rarefaction curves of the observed ASVs of the (C) bacterial and (D) fungal community associated with the colonche stages and fermentation practices.

Supplementary Figure 2 | Non-metric multidimensional scaling (NMDS) plots-based (A) on UniFrac unweighted distance of the bacterial community structure; (B) and the fungal community structure associated with inoculated and spontaneous fermentation practices in the colonche production.

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