Main Challenges Expected from the Impact of Climate Change on Microbial Biodiversity of Table Olives: Current Status and Trends
Abstract
:1. Climate Changes and the Climate Emergency
Overview of Climate Change on the Iberian Peninsula
2. Influence of Climate Change on Olive Cultivars
2.1. Table Olives—Trends in Production and Consumption and Preparation Styles
2.2. Impact of Climate Change on Biological Conditions of Olive Cultivars—Consequences on Olive Trees and Crop Yields
2.3. Impact of Climate Changes on the Main Chemical Compounds of Olives
3. Impact of Biological Changes on Table Olive Microbiological Populations
3.1. Microorganisms Involved in Table Olive Fermentations
3.2. Impact of Climate Change on Fruit Composition, Fermentation, Microbial Population, and Product Safety
3.2.1. Microbial Origin Alterations in Table Olives
3.2.2. Effect of Temperature during the Fermentation
Microbial and Physicochemical Characteristics | Total Microbiota Log CFU/mL | Yeasts Log CFU/mL | Enterobacteria Log CFU/mL | pH | Reducing Sugars g/L | Total Phenolic Compounds g Gallic Acid/L | |
---|---|---|---|---|---|---|---|
Fermentation Process | Unprocessed fruits | 4.08 ± 0.30 | 3.33 ± 0.18 | <Detection limit | ND | ND | ND |
Process A | 25 °C | 7.16 ± 0.65 | 6.47 ± 0.17 | 6.49 ± 0.21 | 4.31 ± 0.03 | 0.76 ± 0.07 | 0.28 ± 0.01 |
Process B | 6.46 ± 0.06 | 6.15 ± 0.11 | <Detection limit | 4.54 ± 0.00 | 2.89 ± 0.41 | 0.89 ± 0.00 | |
Process A | 18 °C | 4.93 ± 0.02 | 4.97 ± 0.19 | <Detection limit | 4.31 ± 0.10 | 1.97 ± 0.33 | 0.29 ± 0.02 |
Process B | 5.15 ± 0.11 | 5.16 ± 0.31 | <Detection limit | 4.51 ± 0.04 | 12.31 ± 1.37 | 1.09 ± 0.07 |
4. Effect of Climate Change on Plagues and Diseases
5. Economic Impact of Climate Change on the Olive Sector
6. Climate Adaptation Measures
6.1. Selection of Resilient Varieties
6.2. Measures during Fermentation
7. Conclusions
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
References
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Year | Temperature (°C) | Average Rainfall (L/m2/Year) | Fermentation Control Parameters | |||
---|---|---|---|---|---|---|
Maximum | Minimum | Average | Rainfall | pH | Free Acidity (%) | |
2019 | 25.40 ± 7.14 | 11.30 ± 5.87 | 18.35 ± 9.61 | 0.93 ± 3.99 | 4.16 ± 0.19 | 0.90 ± 0.25 |
2020 | 25.97 ± 7.76 | 12.36 ± 5.66 | 19.16 ± 9.61 | 1.04 ± 3.52 | 4.25 ± 0.07 | 1.01 ± 0.05 |
2021 | 26.33 ± 7.86 | 12.69 ± 5.89 | 19.51 ± 9.73 | 1.03 ± 3.64 | 4.44 ± 0.21 | 0.85 ± 0.15 |
2022 | 27.96 ± 8.01 | 13.46 ± 5.94 | 20.71 ± 10.12 | 0.90 ± 3.61 | 4.36 ± 0.08 | 0.76 ± 0.04 |
Microbial Groups of Interest | Occurrence or Survival in Table Olives | Relevant Characteristics That Increase Microbial Risks in the Scenario of Climate Issues |
---|---|---|
Bacillus cereus (Main source/origin: soil, dust, vegetation) | Survival in Spanish-style Conservolea olives [84]. | Heterogeneous species comprising psychrotrophic and mesophilic strains (which grow at 37 °C) that can survive at temperatures below 10 °C. Producer of endospores and biofilms. Spores survive in severe conditions (heating, freezing, drying, and ultraviolet) that generally destroy vegetative cells [85]. |
Campylobacter Main source/origin: soil, dust, vegetation | Detected in fruit biofilms from commercialized table olive packaging by metataxonomic analysis [86]. | Considered thermophilic, Campylobacter grows better at high temperatures. It can grow and multiply more rapidly in temperatures between 20 °C and 45 °C. Prolonged storage of unpasteurized foods at inappropriate temperatures, such as within the mentioned range of temperate temperatures, can allow the growth of Campylobacter in the food. |
Clostridium sp. (C. botulinum, C. perfringens) Main source/origin: soil, animals, dust, air, water | Part of fruit microbiota at the beginning of fermentation [87]. Associated with table olives and recalls of the suspected products have been reported [88]. Sulphite-reducing Clostridium spores were detected in numerous samples of commercialized table olives [88]. Clostridium (species not specified) were found in the fermentation of Bella di Cerignola table olives [89]. | C. botulinum: Physiologically heterogeneous species. Producer of endospores and neurotoxins. Proteolytic strains (PS): Optimum growth temperature 37 °C-42 °C. Minimum growth pH: 4.6 Non-proteolytic strains (NPS): Optimum growth temperature 25 °C. Minimum growth pH: 5 NaCl concentration preventing growth: PS: 10%; NPS 5% PS: Inadequate heat treatment will permit the survival of spores that will germinate/grow and produce neurotoxin during ambient storage. NPS: time and/or temperature abuse of commercial or home-made refrigerated foods [90]. C. perfringens: Producer of endospores and endotoxins. Optimal conditions for food poisonings arise when food contaminated with spores is slowly chilled or held in a temperature range of 10–54 °C, allowing germination and rapid growth of C. perfringens. Upon ingestion of large numbers of vegetative C. perfringens cells, they sporulate in the intestinal lumen and produce endotoxins [91]. |
Pathogenic Enterobacteria, e.g., Escherichia coli O157:O7 Main source/origin: water, animal stools. Fecal matter can contaminate food and water, including irrigation water and recreational water. | Survival in table olives of Halkidiki variety [92]. Survival in table olives of different varieties [93]. Survival in Spanish-style Conservolea olives [60]. | E. coli grow from 4 °C to 50 °C, with an optimum at 37 °C. The pathogenicity of E. coli has been explained by the acquisition of a series of virulence genes [94]. The ability of E. coli strains to survive and grow in environments other than the gastrointestinal tract poses a serious public health problem. E. coli was isolated from soil, manure, and irrigation water, and demonstrated the ability to colonize the internal compartments of plants [95] and plant roots [96]. Vegetal material can contribute to the dissemination of bacteria in industrial food processing and packaging environments, contributing to their dissemination in the food chain if good manufacturing practices are not respected. E. coli O157:H7 has the ability to survive and multiply outside the intestine. In table olives, the elimination of pathogenic E. coli is facilitated by a synergy of factors (lactate, phenolics, aW, bacteriocins) related to the overgrowth of preselected starter cultures [97,98]. |
Listeria monocytogenes Main source/origin: soil, animals, insects, compost, decaying vegetation, processing environments. Persist in mammalian and avian feces | Has been found in marketed table olives in Europe, such as Spanish-style process green Nocellara dell’Etna olives [99,100]. Associated with fermented olives with and without starter cultures from different Greek, Italian, and Spanish varieties and fermentation styles [92,99,100]. Survival in table olives of different varieties [94,95,100]. | Psychrotrophic growing at temperatures less than 1 °C to 37 °C. Tolerates NaCl concentration up to 10%, pH < 4, as well as phenolic compounds to a certain extent. Producer of biofilms. Data from Caggia (2004) [100] suggest that L. monocytogenes grow in fermenting brines and can be more probable when the pH is higher (>4.5) and total phenolic and LAB counts are low. Survival under stressful conditions for long periods (+7 months) was reported by several authors. The ability to survive and grow in multiple habitats is supported by a competent system of adaptation to various stresses [101,102]. The ability to grow at refrigerated temperatures makes this bacteria an actual problem for the food industry and consumers during long storage, even at refrigeration temperatures. |
Salmonella sp. Main source/origin: animal stools, human carriers | Survival in black table olive varieties [103]; survival in table olives of different varieties [92,93]. | Salmonella growth ranges from 5 °C to 47 °C, with an optimum at 37 °C. Numerous studies have demonstrated the survival and growth of Salmonella spp. in foods of vegetal origin. Salmonella sp. survives well on low aW foods, such as spices and aromatic herbs, which may eventually be used to season table olives. High lipid concentrations seem to have a protective effect on Salmonella in low aW conditions [104]. Nascimento et al. [105] warned that high levels of lipids protect Salmonella from stomach acidity. Temperature abuses of food products containing Salmonella sp. as a result of contamination or cross-contamination may promote its proliferation, especially during storage at inadequate temperatures. |
Enterobacter cloacae | Isolated from Italian table olives “Bella di Cerignola” [106]. | High temperatures, particularly above 30 °C, favored the proliferation of Enterobacter cloacae. |
Staphylococcus sp. and coagulase positive (S. aureus) Main source/origin: human skin, nasal passages, injuries, environment, surfaces | Part of fruit microbiota at the beginning of fermentation. Enumerated in table olive samples from Portuguese open-air markets [107] and Aloreña de Málaga [108]. Detected in the microbial biofilm that covers the fruit, in marketed samples from different varieties and geographical origins of commercialized table olives [86]. Survival in table olives of different varieties [93]. Survival in commercial Aloreña de Málaga table olives [98]. | S. aureus is one of the most resistant non-spore-forming human pathogens, and can survive for long periods in stressful conditions. Staphylococci are mesophilic. S. aureus growth ranges from 7 °C to 47.8 °C, with an optimum at 35 °C. The growth pH range is between 4.5 and 9.3 (optimum 7.0–7.5). Staphylococci are able to grow at low levels of aW (0.83). Strains of S. aureus are highly tolerant to salts and sugars. Some strains are resistant to multiple antibiotics and may produce (and attach to) biofilms. Temperature abuses of food products containing S. aureus may be responsible for its growth and subsequent production of enterotoxin which can be involved in staphylococcal food poisoning [109]. |
Vibrio sp. Main source/origin: contaminated waters, salt | Part of microbiota at the beginning of fermentation. Detected in the microbial biofilm that covers the fruit, in marketed samples from different varieties and geographical origins [86]. | Vibrio growth ranges from 4 °C to 40 °C, with an optimal of 20–30 °C. Growth occurs at NaCl concentrations of 0–10%, with minimum requirements between 1 and 3.5% (halophilic species). |
Bacteriophages Main source/origin: water, air, vegetables | Viruses that infect strains of L. plantarum species from table olive fermentation were isolated from natural green olives [110]. | High temperatures and bacteriophages can indirectly select pathogenic bacteria in environmental reservoirs [111]. |
Microbial Groups of Interest | Occurrence or Survival in Table Olives | Relevant Characteristics That Increase Microbial Risks in the Scenario of Climate Issues |
---|---|---|
Celerinatantimonas sp. Main source/origin: salt, salty waters | Associated with the gas pocket formation and quality of Spanish-style green olives [69]. Detected in Aloreña de Málaga table olives [97,108]. | Growth ranges from 17 to 49 °C, with optimal at 31 °C, and occurs at NaCl concentrations of 2.5–8.0%, with optimal growth at 7.0–7.5% (halophilic species) [69]. |
Enterobacteriaceae E. coli (non-pathogenic strains) Main source/origin: water, animal stools | Part of fruit microbiota at the beginning of fermentation. Detected at the beginning of fermentation [71,112]. Coliforms and E. coli were enumerated in a few samples of commercialized table olives [107]. | Facultative anaerobic group of microorganisms. Enterobacteriaceae are a good indicator of compliance with good hygiene practices. Its presence in fermented/processed olives means that the fermentation occurred inadequately or that contamination occurred after processing. They are also indicators of adequate washing and sanitization in products of vegetable origin and ready-to-eat foods, such as table olives. High numbers of Enterobacteriaceae represent a risk of deterioration due to the production of off-flavors and gas pocket spoilage on the olives’ surface. Some members of this group may contribute to biogenic amine formation [13]. Their survival decreases when starters are used [112]. Some strains may acquire pathogenic genes (pathogenic E. coli) |
Fungi (e.g., mycotoxins producers Aspergillus sp., Penicillium sp., Alternaria) Main source/origin: soil, dust, air, water | Part of fruit microbiota at the beginning of fermentation. Filamentous fungi are found in bulk and packed table olives. They are easily detectable at the surface and/or by the sensorial changes they cause. Its presence can result in product recalls even if the risk ends up being low [113]. Penicillium sp. in black table olives [114]. Alternaria sp. and Penicillium sp. in Greek cultivars [115]. Penicillium sp. in packed table olives Aloreña de Málaga [97]. Alternaria sp. in brined olives from different countries [116]. Mycotoxins: Aflatoxin B1 was reported in black and green olives of Greek origin [117]; Aflatoxin B1 and ochratoxin A were detected in green Italian table olives [118]. Ochratoxin A, citrinin and aflatoxin B1 were detected in natural black table olives of Moroccan origin [119]. | Physiologically heterogeneous group globally and ubiquitously distributed, isolated from various habitats. They prefer acidic media (able to grow in pH 2.0) and aerobic conditions, but can also grow in the absence of oxygen. As mesophilic organisms (10–40 °C), however, there are thermotolerant species capable of growing at 50 °C. Climate change is contributing to modifying the geographical distribution of fungi, providing new biotic interactions, food contamination pathways, and production of mycotoxins (neurotoxic and carcinogenic) and infections. |
Pseudomonas sp. Main source/origin: ubiquitous, including soil and water. | Detected at different fermentation times in Aloreña de Málaga table olives [108,120] and other varieties [86]. Detected in table olive dressing and seasoning material [121]. Detected in commercialized table olive packages [86]. | Pseudomonas–host interaction could be affected by climate change [122]. Under laboratory conditions, most Pseudomonas species grow at an optimal range from 25 to 30 °C. However, some strains can develop in both warm and cold environments, at temperatures between 0 and 45 °C, depending on the species [123]. |
Other Emergent risks Main source/origin: microorganisms that would adapt to climate changes as eukaryotes, prokaryotes, and viruses in biofilms attached to plastic debris/microplastics (MP) impacting ecosystems | [124,125] | Plastic debris is becoming ubiquitous, and certain species are more likely to integrate biofilms in this so-called “plastisphere”. These include eukaryotic (protozoan and helminth) pathogens that may be associated with bacteria, in which there seems to be a tendency for the predominance of human pathogens. The plastisphere can constitute a new niche with a particular microbial ecology that may cause systemic changes [125]. |
Preventive/Mitigation Measures | Operations/Actions |
---|---|
Raw materials | Hygienic quality of olives and their microenvironment |
Hygienic quality seasonings (herbs and spices, among others) | |
Hygienic quality of salt | |
Use of good quality water | Debittering |
Washing | |
Brining | |
Preparation of authorized additives and technological auxiliaries | |
Disinfection | |
Fermentation | Select adequate starter mixtures (including LAB and yeasts) to better control fermentation |
Monitor fermentation process: pH, acidity, salt, and microbial hygiene parameters | |
Apply corrective measures when needed (brine changes, acidification, salt increase, etc.) | |
Avoid temperature abuse in the supply chain | Storing |
Transport | |
Distribution | |
Commercialization | |
In restaurants, hotels, and at home | |
Selection of hygienic-designed equipment and infrastructures | Processing plants with a hygienic architecture, |
Choose hygiene-designed equipment (fermenters, contains, and conveyor belts) | |
Fermenters and containers without corners, joints, or right angles | |
Filters/incoming air | |
Selection of cleaning and disinfection plans with the appropriate frequency | Avoid microbial biofilms and limit aerosols development in the industries, equipment, and working surfaces |
Adoption of good manufacturing procedures | Prevent contamination and cross-contamination |
Stimulate the adoption of strict personal hygiene | |
Provide education for food handlers | |
Implement or adapt HACCP principles | |
Review/adaptation of HACCP principles | Verify critical points |
Review/adapt critical limits | |
Check conformity regularly by measuring adequate parameters (pH, microbial, and physicochemical limits) | |
Implement corrective measures when a specific critical control point is uncontrolled | |
Regular verification | |
Maintain updated reports | |
Fermentative or beneficial microorganisms capable of | Fermentation abilities that produce acids, contribute to the lowering of pH and produce flavor compounds |
Producing antimicrobial compounds (bacteriocins) | |
Establishing new biotic interactions | |
Internalizing the mesocarp/pulp of the table olives | |
Improving the nutritional properties of table olives, notably their vitamin content | |
Contributing to the decrease in occurrence of toxins | |
Giving origin to probiotic and postbiotic in the final products |
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Benítez-Cabello, A.; Delgado, A.M.; Quintas, C. Main Challenges Expected from the Impact of Climate Change on Microbial Biodiversity of Table Olives: Current Status and Trends. Foods 2023, 12, 3712. https://doi.org/10.3390/foods12193712
Benítez-Cabello A, Delgado AM, Quintas C. Main Challenges Expected from the Impact of Climate Change on Microbial Biodiversity of Table Olives: Current Status and Trends. Foods. 2023; 12(19):3712. https://doi.org/10.3390/foods12193712
Chicago/Turabian StyleBenítez-Cabello, Antonio, Amélia M. Delgado, and Célia Quintas. 2023. "Main Challenges Expected from the Impact of Climate Change on Microbial Biodiversity of Table Olives: Current Status and Trends" Foods 12, no. 19: 3712. https://doi.org/10.3390/foods12193712