Pub Date : 2023-10-26DOI: 10.1186/s13213-023-01740-9
Desalegn Amenu, Ketema Bacha
Abstract Background Probiotics are live microorganisms that effectively combat foodborne pathogens, promoting intestinal health when consumed in sufficient amounts. This study evaluated the probiotic potential and safety of lactic acid bacteria isolated from selected Ethiopian traditional fermented foods and beverages (Kotcho, Bulla, Ergo, Cabbage-Shamita, Borde, and Bukuri). To assess the isolates’ probiotic activity, tolerance, and survival rate under various stressful conditions, including low pH, intestinal inhibitory substances, salt concentration, bile salt, and simulated gastric/intestinal juice. The isolates were also tested for antagonistic activities against common bacterial and fungal pathogens ( Staphylococcus aureus , Salmonella Typhimurium, Escherichia coli , Pseudomonas aeruginosa , Klebsiella pneumoniae , and Candida albicans ) and safety (auto-aggregation, co-aggregation, cell source hydrophobicity, hemolytic activity, DNase, and antibiotic susceptibility). The best probiotic lactic acid bacteria (LAB) were characterized to species level following standard MALDI TOF/mass spectrometry analysis. Results A total of 125 potentially probiotic LAB were isolated of which 17 (13.60%) isolates survived low pH (2, 2.5, and 3), bile salt (0.3%), intestinal inhibitory chemicals (phenol, bile, low acidity, pepsin, and pancreas), and simulated gastro-intestinal settings with near 60–94% survival rate. In addition, 11 best LAB isolates were further screened based on additional screening including their antimicrobial efficacy, preservative efficiency, bacteriocin production besides resistance to low acid and bile salts, and survival potential under simulated gastrointestinal conditions. All 11 LAB isolates were resistant to ampicillin, vancomycin, gentamicin, kanamycin, clindamycin, and chloramphenicol, while they were susceptible to streptomycin and tetracycline. The MALDI TOF mass spectrometry analysis result of efficient probiotic LAB grouped them under the genus Pediococcu s, Enterococcus , and Lactococcus including Pediococcus pentosaceus , Enterococcus faecium , Lactococcus lactis , and Pediococcus acidilactici . Conclusion Ethiopian traditional fermented foods and beverages are good sources of promising probiotic lactic acid bacteria. These isolates could serve as potential starter cultures and bio-preservative for the enhancement of the shelf life of foods. This study established the groundwork for the selection of excellent probiotics for the development and application of LAB for antibacterial action, starter culture production, and preservation activities.
{"title":"Probiotic potential and safety analysis of lactic acid bacteria isolated from Ethiopian traditional fermented foods and beverages","authors":"Desalegn Amenu, Ketema Bacha","doi":"10.1186/s13213-023-01740-9","DOIUrl":"https://doi.org/10.1186/s13213-023-01740-9","url":null,"abstract":"Abstract Background Probiotics are live microorganisms that effectively combat foodborne pathogens, promoting intestinal health when consumed in sufficient amounts. This study evaluated the probiotic potential and safety of lactic acid bacteria isolated from selected Ethiopian traditional fermented foods and beverages (Kotcho, Bulla, Ergo, Cabbage-Shamita, Borde, and Bukuri). To assess the isolates’ probiotic activity, tolerance, and survival rate under various stressful conditions, including low pH, intestinal inhibitory substances, salt concentration, bile salt, and simulated gastric/intestinal juice. The isolates were also tested for antagonistic activities against common bacterial and fungal pathogens ( Staphylococcus aureus , Salmonella Typhimurium, Escherichia coli , Pseudomonas aeruginosa , Klebsiella pneumoniae , and Candida albicans ) and safety (auto-aggregation, co-aggregation, cell source hydrophobicity, hemolytic activity, DNase, and antibiotic susceptibility). The best probiotic lactic acid bacteria (LAB) were characterized to species level following standard MALDI TOF/mass spectrometry analysis. Results A total of 125 potentially probiotic LAB were isolated of which 17 (13.60%) isolates survived low pH (2, 2.5, and 3), bile salt (0.3%), intestinal inhibitory chemicals (phenol, bile, low acidity, pepsin, and pancreas), and simulated gastro-intestinal settings with near 60–94% survival rate. In addition, 11 best LAB isolates were further screened based on additional screening including their antimicrobial efficacy, preservative efficiency, bacteriocin production besides resistance to low acid and bile salts, and survival potential under simulated gastrointestinal conditions. All 11 LAB isolates were resistant to ampicillin, vancomycin, gentamicin, kanamycin, clindamycin, and chloramphenicol, while they were susceptible to streptomycin and tetracycline. The MALDI TOF mass spectrometry analysis result of efficient probiotic LAB grouped them under the genus Pediococcu s, Enterococcus , and Lactococcus including Pediococcus pentosaceus , Enterococcus faecium , Lactococcus lactis , and Pediococcus acidilactici . Conclusion Ethiopian traditional fermented foods and beverages are good sources of promising probiotic lactic acid bacteria. These isolates could serve as potential starter cultures and bio-preservative for the enhancement of the shelf life of foods. This study established the groundwork for the selection of excellent probiotics for the development and application of LAB for antibacterial action, starter culture production, and preservation activities.","PeriodicalId":8069,"journal":{"name":"Annals of Microbiology","volume":"19 4","pages":"0"},"PeriodicalIF":0.0,"publicationDate":"2023-10-26","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"134909954","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":4,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2023-10-14DOI: 10.1186/s13213-023-01738-3
Arifa Akhter Airin, Md Iyasir Arafat, Rifat Ara Begum, Md Rakibul Islam, Zeba Islam Seraj
Abstract Background Plant growth-promoting endophytic fungi (PGPEF) that are associated with halophytes have the potential to boost crop salinity tolerance and productivity. This in turn has the potential of enabling and improving cultivation practices in coastal lands affected by salt stress. Methods Endophytic fungi from the wild halophytic rice Oryza coarctata were isolated, characterized, identified, and studied for their effects on all developing stages of rice plant growth and their yields both with and without salt stress. Key results In this study, three different fungal endophytes were isolated from the halophytic wild rice Oryza coarctata . Two isolates were identified as Talaromyces adpressus (OPCRE2) and Talaromyces argentinensis (OPCRh1) by ITS region sequencing. The remaining isolate NPCRE2 was confirmed as a novel strain named Aspergillus welwitschiae Oc streb1 ( AwOc streb1) by whole genome sequencing. These endophytes showed various plant growth-promoting (PGP) abilities in vitro (e.g., IAA, ACC-deaminase and siderophore production, phosphate, and zinc solubilization as well as nitrogen fixation), where AwOc streb1 was significantly more efficient compared to the other two isolates at high salinity (900 mm). Independent application of these fungi in commercial rice ( Oryza sativa ) showed significant elevation in plant growth, especially in the case of the AwOc streb1 inoculants, which had enhanced metabolite and chlorophyll content at the seedling stage in both no-salt control and 100-m m salt-stressed plants. At the same time, AwOc streb1-treated plants had a significantly lower level of H 2 O 2 , electrolyte leakage, and Na + /K + ratio under saline conditions. Higher expression (1.6 folds) of the SOS1 (salt overly sensitive 1) gene was also observed in these plants under salinity stress. This strain also improved percent fertility, tillering, panicle number, and filled grain number in both no-salt control and 45-m m salt-stressed inoculated plants at the reproductive stage. Consequently, the differences in their yield was 125.16% and 203.96% ( p < 0.05) in colonized plants in normal and saline conditions, respectively, compared to uninoculated controls. Conclusions We propose that AwOc streb1 is a potential candidate for an eco-friendly biofertilizer formula to improve the cultivation and yield of rice or any other crop in the highly saline coastal regions of Bangladesh.
{"title":"Plant growth-promoting endophytic fungi of the wild halophytic rice Oryza coarctata","authors":"Arifa Akhter Airin, Md Iyasir Arafat, Rifat Ara Begum, Md Rakibul Islam, Zeba Islam Seraj","doi":"10.1186/s13213-023-01738-3","DOIUrl":"https://doi.org/10.1186/s13213-023-01738-3","url":null,"abstract":"Abstract Background Plant growth-promoting endophytic fungi (PGPEF) that are associated with halophytes have the potential to boost crop salinity tolerance and productivity. This in turn has the potential of enabling and improving cultivation practices in coastal lands affected by salt stress. Methods Endophytic fungi from the wild halophytic rice Oryza coarctata were isolated, characterized, identified, and studied for their effects on all developing stages of rice plant growth and their yields both with and without salt stress. Key results In this study, three different fungal endophytes were isolated from the halophytic wild rice Oryza coarctata . Two isolates were identified as Talaromyces adpressus (OPCRE2) and Talaromyces argentinensis (OPCRh1) by ITS region sequencing. The remaining isolate NPCRE2 was confirmed as a novel strain named Aspergillus welwitschiae Oc streb1 ( AwOc streb1) by whole genome sequencing. These endophytes showed various plant growth-promoting (PGP) abilities in vitro (e.g., IAA, ACC-deaminase and siderophore production, phosphate, and zinc solubilization as well as nitrogen fixation), where AwOc streb1 was significantly more efficient compared to the other two isolates at high salinity (900 mm). Independent application of these fungi in commercial rice ( Oryza sativa ) showed significant elevation in plant growth, especially in the case of the AwOc streb1 inoculants, which had enhanced metabolite and chlorophyll content at the seedling stage in both no-salt control and 100-m m salt-stressed plants. At the same time, AwOc streb1-treated plants had a significantly lower level of H 2 O 2 , electrolyte leakage, and Na + /K + ratio under saline conditions. Higher expression (1.6 folds) of the SOS1 (salt overly sensitive 1) gene was also observed in these plants under salinity stress. This strain also improved percent fertility, tillering, panicle number, and filled grain number in both no-salt control and 45-m m salt-stressed inoculated plants at the reproductive stage. Consequently, the differences in their yield was 125.16% and 203.96% ( p < 0.05) in colonized plants in normal and saline conditions, respectively, compared to uninoculated controls. Conclusions We propose that AwOc streb1 is a potential candidate for an eco-friendly biofertilizer formula to improve the cultivation and yield of rice or any other crop in the highly saline coastal regions of Bangladesh.","PeriodicalId":8069,"journal":{"name":"Annals of Microbiology","volume":"31 1","pages":"0"},"PeriodicalIF":0.0,"publicationDate":"2023-10-14","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"135766633","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":4,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2023-10-13DOI: 10.1186/s13213-023-01739-2
Mohamed El-Khateeb, Gamal K. Hassan, Mohamed Azab El-Liethy, Kamel M. El-Khatib, Hussein I. Abdel-Shafy, Anyi Hu, Mahmoud Gad
Abstract Background The upflow anaerobic sludge blanket (UASB) reactors rely on bacterial communities to break down pollutants in wastewater (municipal or industrial). Methods and results In this study, a novel combination of UASB followed by aerobic treatment has been proposed for the treatment of municipal wastewater focusing on bacterial communities using high-throughput sequencing and parasite removal in this novel combination of reactors. Moreover, economic estimation of the compact unit composed of two overlapping UASB reactors, followed by a downflow hanging non-woven fabric (DHNW) reactor, the anaerobic baffled reactor (ABR), and chlorine unit was investigated in this study based on community populations of 1000 and 10,000 inhabitants, with a municipal plant capacity of 54,000 and 540,000 m 3 /year. Cost estimation was conducted based on two scenarios, one considering the contingency cost and auxiliary facility, and the other excluding them. Non-metric multidimensional scaling (nMDS) revealed that the treatment stages structured the microbial communities. Proteobacteria was the most prevalent phylum in all treatment stages, followed by Bacteroidota in most stages. Firmicutes and Actinobacteria were also present in significant amounts. The treatment system achieved from 40 to 66.67% removal of parasites (parasitic nematode, Cryptosporidium , and microsporidia). Redundancy analysis (RDA) indicated a strong positive correlation between chemical and biological oxygen demand (COD/BOD) with Campylobacterales and could be used as a bioindicator of treatment performance. Conclusion These findings can inform the development of more efficient and sustainable wastewater treatment systems that take into account microbial ecology and economic considerations.
{"title":"Sustainable municipal wastewater treatment using an innovative integrated compact unit: microbial communities, parasite removal, and techno-economic analysis","authors":"Mohamed El-Khateeb, Gamal K. Hassan, Mohamed Azab El-Liethy, Kamel M. El-Khatib, Hussein I. Abdel-Shafy, Anyi Hu, Mahmoud Gad","doi":"10.1186/s13213-023-01739-2","DOIUrl":"https://doi.org/10.1186/s13213-023-01739-2","url":null,"abstract":"Abstract Background The upflow anaerobic sludge blanket (UASB) reactors rely on bacterial communities to break down pollutants in wastewater (municipal or industrial). Methods and results In this study, a novel combination of UASB followed by aerobic treatment has been proposed for the treatment of municipal wastewater focusing on bacterial communities using high-throughput sequencing and parasite removal in this novel combination of reactors. Moreover, economic estimation of the compact unit composed of two overlapping UASB reactors, followed by a downflow hanging non-woven fabric (DHNW) reactor, the anaerobic baffled reactor (ABR), and chlorine unit was investigated in this study based on community populations of 1000 and 10,000 inhabitants, with a municipal plant capacity of 54,000 and 540,000 m 3 /year. Cost estimation was conducted based on two scenarios, one considering the contingency cost and auxiliary facility, and the other excluding them. Non-metric multidimensional scaling (nMDS) revealed that the treatment stages structured the microbial communities. Proteobacteria was the most prevalent phylum in all treatment stages, followed by Bacteroidota in most stages. Firmicutes and Actinobacteria were also present in significant amounts. The treatment system achieved from 40 to 66.67% removal of parasites (parasitic nematode, Cryptosporidium , and microsporidia). Redundancy analysis (RDA) indicated a strong positive correlation between chemical and biological oxygen demand (COD/BOD) with Campylobacterales and could be used as a bioindicator of treatment performance. Conclusion These findings can inform the development of more efficient and sustainable wastewater treatment systems that take into account microbial ecology and economic considerations.","PeriodicalId":8069,"journal":{"name":"Annals of Microbiology","volume":"76 1","pages":"0"},"PeriodicalIF":0.0,"publicationDate":"2023-10-13","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"135857084","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":4,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2023-09-28DOI: 10.1186/s13213-023-01736-5
Muhammad Ahmad, Muhammad Imtiaz, Muhammad Shoib Nawaz, Fathia Mubeen, Yasra Sarwar, Mahnoor Hayat, Muhammad Asif, Rubab Zahra Naqvi, Muhammad Ahmad, Asma Imran
Abstract Background Global warming and irregular changes in temperature are a serious threat to plant growth with a significant negative impact on yield. Global maize productivity has decreased significantly due to sudden temperature fluctuations and heat waves especially in the regions severely hit by climate change. Results The current study demonstrates the potential of beneficial bacteria for inducing heat tolerance in maize during early growth. Three Bacillus spp . AH-08, AH-67, SH-16, and one Pseudomonas spp . SH-29 showed the ability to grow and exhibited multiple plant-beneficial traits up to 45 ± 2 °C. At temperatures of 45 and 50 °C, Bacillus sp. SH-16 exhibited upregulation of two small heat shock proteins (HSP) of 15 and 30 kDa, while SH-16 and AH-67 showed upregulation of two large HSP of 65 and 100 kDa. Plant-inoculation with the consortium B3P (3 Bacillus + 1 Pseudomonas spp.) was carried out on six hybrid maize varieties pre-grown at 25 ± 2 ºC. Heat shock was applied to 10-day-old seedlings as: 3 h at 38ºC, 48 h recovery period, and then 48 h at 42ºC. The B3P treatment showed significant improvement in the overall plant growth (plant height, root & shoot fresh & dry weight, root and leaf area) with a higher level of CAT, POD, total chlorophyll, and carotenoids, while low concentration of MDA. A non-significant difference was observed in case of total cell protein and amino acids after B3P-treatment under stress. The expression of HSP1 and HSP18 in Malka and YH-5427 while HSP70 and HSP101 were higher in FH-1046 and Gohar as compared to non-inoculated treatment. Conclusions These findings indicate that heat-tolerant plant-growth promoting rhizobacteria (Ht-PGPR) exert versatile, multiphasic and differential response to improve plant growth and heat-tolerance in different maize varieties during seedling/ early vegetative growth. Subsequent research will be focused on the field evaluation of these PGPR to see the field and yield response of this consortium under natural temperature fluctuations in field.
{"title":"Thermotolerant PGPR consortium B3P modulates physio-biochemical and molecular machinery for enhanced heat tolerance in maize during early vegetative growth","authors":"Muhammad Ahmad, Muhammad Imtiaz, Muhammad Shoib Nawaz, Fathia Mubeen, Yasra Sarwar, Mahnoor Hayat, Muhammad Asif, Rubab Zahra Naqvi, Muhammad Ahmad, Asma Imran","doi":"10.1186/s13213-023-01736-5","DOIUrl":"https://doi.org/10.1186/s13213-023-01736-5","url":null,"abstract":"Abstract Background Global warming and irregular changes in temperature are a serious threat to plant growth with a significant negative impact on yield. Global maize productivity has decreased significantly due to sudden temperature fluctuations and heat waves especially in the regions severely hit by climate change. Results The current study demonstrates the potential of beneficial bacteria for inducing heat tolerance in maize during early growth. Three Bacillus spp . AH-08, AH-67, SH-16, and one Pseudomonas spp . SH-29 showed the ability to grow and exhibited multiple plant-beneficial traits up to 45 ± 2 °C. At temperatures of 45 and 50 °C, Bacillus sp. SH-16 exhibited upregulation of two small heat shock proteins (HSP) of 15 and 30 kDa, while SH-16 and AH-67 showed upregulation of two large HSP of 65 and 100 kDa. Plant-inoculation with the consortium B3P (3 Bacillus + 1 Pseudomonas spp.) was carried out on six hybrid maize varieties pre-grown at 25 ± 2 ºC. Heat shock was applied to 10-day-old seedlings as: 3 h at 38ºC, 48 h recovery period, and then 48 h at 42ºC. The B3P treatment showed significant improvement in the overall plant growth (plant height, root & shoot fresh & dry weight, root and leaf area) with a higher level of CAT, POD, total chlorophyll, and carotenoids, while low concentration of MDA. A non-significant difference was observed in case of total cell protein and amino acids after B3P-treatment under stress. The expression of HSP1 and HSP18 in Malka and YH-5427 while HSP70 and HSP101 were higher in FH-1046 and Gohar as compared to non-inoculated treatment. Conclusions These findings indicate that heat-tolerant plant-growth promoting rhizobacteria (Ht-PGPR) exert versatile, multiphasic and differential response to improve plant growth and heat-tolerance in different maize varieties during seedling/ early vegetative growth. Subsequent research will be focused on the field evaluation of these PGPR to see the field and yield response of this consortium under natural temperature fluctuations in field.","PeriodicalId":8069,"journal":{"name":"Annals of Microbiology","volume":"25 1","pages":"0"},"PeriodicalIF":0.0,"publicationDate":"2023-09-28","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"135342806","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":4,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Abstract Purpose As an invasive plant, Parthenium hysterophorus severely impacts the ecological environment of the Yellow River Delta and reduces biodiversity in the invaded areas. The effects of P. hysterophorus invasion on the local environment became increasingly critical, while few information was available for the effects of P. hysterophorus invasion on soil bacteria. The present study aimed to reveal the impacts of hysterophorus on the fungal communities in the Yellow River Delta. Methods Sixteen soil samples including four groups (ROOT group, YRR group, YNR group, and GBS group) were collected. High-throughput methods were used to explore the fungal composition of the P. hysterophorus -invaded surrounding environment and native plant-growed environment. Results Our results showed that the ACE (351.97) and Chao1 (351.95) values of the rhizosphere soils of P. hysterophorus (YRR group) were the highest among the four groups, whereas the non-rhizosphere soil samples of P. hysterophorus (YNR group) had the highest Shannon (7.188) and Simpson (0.984) values. The total number of operational taxonomic units (OTUs) obtained from the four groups was 1965, with 161 common OTUs among different groups. At the phylum level, both Ascomycota and Basidiomycota were the dominant fungi, with Ascomycota having the highest abundance. At the genus level, except for the endophytic fungi of P. hysterophorus roots (ROOT group), Fusarium , Mortierella , Comoclathris , and Cladosporium were the dominant fungi in three groups. The fungal communities within the roots of P. hysterophorus were distant from other groups, indicating that the composition of the fungal communities within the roots had a low degree of similarity to the other three groups. LEfSe analysis showed that Ascomycota at the phylum level and Cladosporium , Curvularia , and Alternaria at the genus level play essential roles in the ROOT group, and Comoclathris plays a vital role in the YNR group. Conclusions This study explored the effects of P. hysterophorus invasion on the local soil fungal communities by analyzing the fungal communities in P. hysterophorus roots , rhizosphere soil, non-rhizosphere soil, and rhizosphere soil of native plants. Generally, P. hysterophorus rhizosphere fungi specifically affect the surrounding environment.
{"title":"Impact of Parthenium hysterophorus L. invasion on soil fungal communities in the Yellow River Delta","authors":"Lixin Gong, Xin Xin, Wei Song, Zaiwang Zhang, Jiabo Zhang, Shuai Shang","doi":"10.1186/s13213-023-01735-6","DOIUrl":"https://doi.org/10.1186/s13213-023-01735-6","url":null,"abstract":"Abstract Purpose As an invasive plant, Parthenium hysterophorus severely impacts the ecological environment of the Yellow River Delta and reduces biodiversity in the invaded areas. The effects of P. hysterophorus invasion on the local environment became increasingly critical, while few information was available for the effects of P. hysterophorus invasion on soil bacteria. The present study aimed to reveal the impacts of hysterophorus on the fungal communities in the Yellow River Delta. Methods Sixteen soil samples including four groups (ROOT group, YRR group, YNR group, and GBS group) were collected. High-throughput methods were used to explore the fungal composition of the P. hysterophorus -invaded surrounding environment and native plant-growed environment. Results Our results showed that the ACE (351.97) and Chao1 (351.95) values of the rhizosphere soils of P. hysterophorus (YRR group) were the highest among the four groups, whereas the non-rhizosphere soil samples of P. hysterophorus (YNR group) had the highest Shannon (7.188) and Simpson (0.984) values. The total number of operational taxonomic units (OTUs) obtained from the four groups was 1965, with 161 common OTUs among different groups. At the phylum level, both Ascomycota and Basidiomycota were the dominant fungi, with Ascomycota having the highest abundance. At the genus level, except for the endophytic fungi of P. hysterophorus roots (ROOT group), Fusarium , Mortierella , Comoclathris , and Cladosporium were the dominant fungi in three groups. The fungal communities within the roots of P. hysterophorus were distant from other groups, indicating that the composition of the fungal communities within the roots had a low degree of similarity to the other three groups. LEfSe analysis showed that Ascomycota at the phylum level and Cladosporium , Curvularia , and Alternaria at the genus level play essential roles in the ROOT group, and Comoclathris plays a vital role in the YNR group. Conclusions This study explored the effects of P. hysterophorus invasion on the local soil fungal communities by analyzing the fungal communities in P. hysterophorus roots , rhizosphere soil, non-rhizosphere soil, and rhizosphere soil of native plants. Generally, P. hysterophorus rhizosphere fungi specifically affect the surrounding environment.","PeriodicalId":8069,"journal":{"name":"Annals of Microbiology","volume":"9 1","pages":"0"},"PeriodicalIF":0.0,"publicationDate":"2023-09-20","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"136308717","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":4,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2023-09-19DOI: 10.1186/s13213-023-01727-6
Xu Gao, Mengjiao Ding, Tao Wu, Xiaohua Deng, Qiang Li
Abstract Purpose Soil microbial communities are critically important to agricultural ecosystems. The present study aimed to evaluate the changes in soil microbial community composition and functional groups after planting Phallus rubrovolvatus . Methods Illumina platform were adopted to characterize the bacterial and fungal diversity in the soil cropped with P. rubrovolvatus for 0 and 1 year. Results The results showed that planting P. rubrovolvatus reduced the bacterial and fungal diversity in the soil, and the dynamics of the soil bacterial diversity changed more drastically. This study also indicated that, as keystone taxa, the dominant bacteria ( Actinobacteria , Sphingomonas , Xanthobacteraceae , and Gemmatimonadaceae ) and dominant fungi ( Mortierellales and Eurotiales ) served as a key component in the network of soil microbial communities. Moreover, the bacterial and fungal communities in the soil planted with P. rubrovolvatus formed more similar and weak networks. Conclusion Planting P. rubrovolvatus significantly influenced the structure and composition of microbial communities. In the future, we will focus on ways to improve the soil environment after planting P. rubrovolvatus .
{"title":"Impact of planting Phallus rubrovolvatus on physicochemical and microbial properties and functional groups of soil","authors":"Xu Gao, Mengjiao Ding, Tao Wu, Xiaohua Deng, Qiang Li","doi":"10.1186/s13213-023-01727-6","DOIUrl":"https://doi.org/10.1186/s13213-023-01727-6","url":null,"abstract":"Abstract Purpose Soil microbial communities are critically important to agricultural ecosystems. The present study aimed to evaluate the changes in soil microbial community composition and functional groups after planting Phallus rubrovolvatus . Methods Illumina platform were adopted to characterize the bacterial and fungal diversity in the soil cropped with P. rubrovolvatus for 0 and 1 year. Results The results showed that planting P. rubrovolvatus reduced the bacterial and fungal diversity in the soil, and the dynamics of the soil bacterial diversity changed more drastically. This study also indicated that, as keystone taxa, the dominant bacteria ( Actinobacteria , Sphingomonas , Xanthobacteraceae , and Gemmatimonadaceae ) and dominant fungi ( Mortierellales and Eurotiales ) served as a key component in the network of soil microbial communities. Moreover, the bacterial and fungal communities in the soil planted with P. rubrovolvatus formed more similar and weak networks. Conclusion Planting P. rubrovolvatus significantly influenced the structure and composition of microbial communities. In the future, we will focus on ways to improve the soil environment after planting P. rubrovolvatus .","PeriodicalId":8069,"journal":{"name":"Annals of Microbiology","volume":"2 1","pages":"0"},"PeriodicalIF":0.0,"publicationDate":"2023-09-19","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"135014225","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":4,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2023-09-16DOI: 10.1186/s13213-023-01734-7
Jili Zhang, Jiayi Song, Jianyu Wei, Shi Qi, Junlin Li, Yabo Jin, Xinbo Luan, Ping Li, Jian Yan
Abstract Background Numerous chemical pesticides have been used in agricultural production to combat crop diseases and pests. Despite ensuring certain economic advantages, they have also resulted in issues like environmental contamination, declining soil quality, and pesticide residues. Because biological control is environmentally friendly and difficult to acquire resistance to, it has been used in practice recently. Methods In this study, we isolated the endophytic fungus Purpureocillium lilacinum from Portulaca oleracea L . , which was previously found to have inhibitory effects on soil pathogens in tobacco fields. To find out how the biocontrol agent P. lilacinum affects soil microorganisms and plant metabolism in tobacco cultivation, we used amplicon sequencing technology and gas chromatography-mass spectrometry to look at the structure of soil microbial communities and the networks of interactions between microorganisms and metabolites in the inter-rhizosphere soil of tobacco fields treated with different amounts of P. lilacinum . Results The findings showed that there was a trend toward less microbial diversity among inter-root microorganisms as solid-state fermentation (SSF) products of P. lilacinum increased; however, submerged fermentation (SmF) had no discernible impact on microbial diversity when compared to the direct use of SSF. Additionally, the relationship between inter-root fungi and volatile compounds in tobacco leaves was dominated by a negative correlation. Conclusions The result demonstrated that P. lilacinum ’s antagonistic interaction in the inter-rhizosphere microbial community was dominant and valuable for biopesticide application. P. lilacinum can work more effectively on tobacco roots by using SSF products. P. lilacinum ’s opposition to fungal colonies may enhance the volatile chemicals in tobacco leaves. These provide some implications for the biocontrol application of P. lilacinum .
摘要背景在农业生产中，为了防治作物病虫害，使用了大量的化学农药。尽管确保了一定的经济优势，但它们也导致了环境污染、土壤质量下降和农药残留等问题。由于生物防治具有环境友好、不易产生抗药性等特点，近年来得到了广泛的应用。方法从马齿苋(Portulaca oleracea L .)中分离得到一种内生真菌紫丁香紫霉(Purpureocillium lilacinum)。在烟草田中发现对土壤病原菌有抑制作用。为了解生物防治剂丁香花对烟草种植中土壤微生物和植物代谢的影响，采用扩增子测序技术和气相色谱-质谱联用技术，研究了不同剂量丁香花处理烟田根际土壤微生物群落结构及微生物与代谢物的相互作用网络。结果随着紫丁香菌固态发酵(SSF)产物的增加，根间微生物多样性呈减少趋势;然而，与直接使用深层发酵相比，深层发酵(SmF)对微生物多样性没有明显的影响。根间真菌与烟叶挥发性物质的关系以负相关为主。结论紫丁香在根际微生物群落中具有拮抗作用，具有一定的生物农药应用价值。使用SSF产品后，紫丁香叶菌对烟草根的作用更有效。紫丁香对真菌菌落的拮抗作用可能会增加烟叶中挥发性化学物质的含量。这些结果对紫丁香菌的生物防治应用具有一定的指导意义。
{"title":"Effect of Purpureocillium lilacinum on inter-root soil microbial community and metabolism of tobacco","authors":"Jili Zhang, Jiayi Song, Jianyu Wei, Shi Qi, Junlin Li, Yabo Jin, Xinbo Luan, Ping Li, Jian Yan","doi":"10.1186/s13213-023-01734-7","DOIUrl":"https://doi.org/10.1186/s13213-023-01734-7","url":null,"abstract":"Abstract Background Numerous chemical pesticides have been used in agricultural production to combat crop diseases and pests. Despite ensuring certain economic advantages, they have also resulted in issues like environmental contamination, declining soil quality, and pesticide residues. Because biological control is environmentally friendly and difficult to acquire resistance to, it has been used in practice recently. Methods In this study, we isolated the endophytic fungus Purpureocillium lilacinum from Portulaca oleracea L . , which was previously found to have inhibitory effects on soil pathogens in tobacco fields. To find out how the biocontrol agent P. lilacinum affects soil microorganisms and plant metabolism in tobacco cultivation, we used amplicon sequencing technology and gas chromatography-mass spectrometry to look at the structure of soil microbial communities and the networks of interactions between microorganisms and metabolites in the inter-rhizosphere soil of tobacco fields treated with different amounts of P. lilacinum . Results The findings showed that there was a trend toward less microbial diversity among inter-root microorganisms as solid-state fermentation (SSF) products of P. lilacinum increased; however, submerged fermentation (SmF) had no discernible impact on microbial diversity when compared to the direct use of SSF. Additionally, the relationship between inter-root fungi and volatile compounds in tobacco leaves was dominated by a negative correlation. Conclusions The result demonstrated that P. lilacinum ’s antagonistic interaction in the inter-rhizosphere microbial community was dominant and valuable for biopesticide application. P. lilacinum can work more effectively on tobacco roots by using SSF products. P. lilacinum ’s opposition to fungal colonies may enhance the volatile chemicals in tobacco leaves. These provide some implications for the biocontrol application of P. lilacinum .","PeriodicalId":8069,"journal":{"name":"Annals of Microbiology","volume":"28 1","pages":"0"},"PeriodicalIF":0.0,"publicationDate":"2023-09-16","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"135307973","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":4,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Abstract Background Subclinical infection with bovine leukemia virus (BLV) in cows can cause economic losses in milk and meat production in many countries, as BLV-related negative effects. The volatile fatty acids (VFAs) and microbiota present in the digestive tracts of cows can contribute to cow health. Here, we exploratorily investigated the VFAs and microbiota in the rumen and gut with respect to subclinical BLV infection using cows housed at a single farm. Results We analyzed a herd of 38 cows kept at one farm, which included 15 uninfected and 23 BLV-infected cows. First, the analysis of the VFAs in the rumen, gut, and blood revealed an absence of statistically significant differences between the uninfected and BLV-infected groups. Thus, BLV infection did not cause major changes in VFA levels in all tested specimens. Next, we analyzed the rumen and gut microbiota. The analysis of the microbial diversity revealed a modest difference between the uninfected and BLV-infected groups in the gut; by contrast, no differences were observed in the rumen. In addition, the investigation of the bacteria that were predominant in the uninfected and BLV-infected groups via a differential abundance analysis showed that no significant bacteria were present in either of the microbiota. Thus, BLV infection possibly affected the gut microbiota to a small extent. Moreover, bacterial associations were compared between the uninfected and BLV-infected groups. The results of this analysis suggested that BLV infection affected the equilibrium of the bacterial associations in both microbiota, which might be related to the BLV-related negative effects. Thus, BLV infection may negatively affect the equilibrium of bacterial associations in both microbiota. Conclusions Subclinical BLV infection is likely to affect the rumen and gut microbiota, which may partly explain the BLV-related negative effects.
{"title":"Exploratory study of volatile fatty acids and the rumen-and-gut microbiota of dairy cows in a single farm, with respect to subclinical infection with bovine leukemia virus","authors":"Takehito Suzuki, Hironobu Murakami, Jumpei Uchiyama, Reiichiro Sato, Iyo Takemura-Uchiyama, Masaya Ogata, Kazuyuki Sogawa, Hiroho Ishida, Apichart Atipairin, Osamu Matsushita, Makoto Nagai","doi":"10.1186/s13213-023-01737-4","DOIUrl":"https://doi.org/10.1186/s13213-023-01737-4","url":null,"abstract":"Abstract Background Subclinical infection with bovine leukemia virus (BLV) in cows can cause economic losses in milk and meat production in many countries, as BLV-related negative effects. The volatile fatty acids (VFAs) and microbiota present in the digestive tracts of cows can contribute to cow health. Here, we exploratorily investigated the VFAs and microbiota in the rumen and gut with respect to subclinical BLV infection using cows housed at a single farm. Results We analyzed a herd of 38 cows kept at one farm, which included 15 uninfected and 23 BLV-infected cows. First, the analysis of the VFAs in the rumen, gut, and blood revealed an absence of statistically significant differences between the uninfected and BLV-infected groups. Thus, BLV infection did not cause major changes in VFA levels in all tested specimens. Next, we analyzed the rumen and gut microbiota. The analysis of the microbial diversity revealed a modest difference between the uninfected and BLV-infected groups in the gut; by contrast, no differences were observed in the rumen. In addition, the investigation of the bacteria that were predominant in the uninfected and BLV-infected groups via a differential abundance analysis showed that no significant bacteria were present in either of the microbiota. Thus, BLV infection possibly affected the gut microbiota to a small extent. Moreover, bacterial associations were compared between the uninfected and BLV-infected groups. The results of this analysis suggested that BLV infection affected the equilibrium of the bacterial associations in both microbiota, which might be related to the BLV-related negative effects. Thus, BLV infection may negatively affect the equilibrium of bacterial associations in both microbiota. Conclusions Subclinical BLV infection is likely to affect the rumen and gut microbiota, which may partly explain the BLV-related negative effects.","PeriodicalId":8069,"journal":{"name":"Annals of Microbiology","volume":"19 1","pages":"0"},"PeriodicalIF":0.0,"publicationDate":"2023-09-16","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"135308611","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":4,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Abstract Purpose This study aims to explore the effects of two endophytes of Epimedium koreanum Nakai on host plant growth and development and medicinal material quality and to promote the growth and development of ingredients derived from Epimedium koreanum Nakai . Methods The effects on the biomass, photosynthesis parameters, chlorophyll fluorescence parameters, activity of key enzymes, and active components in the process of growth and development in Korea were examined. Results From the analysis of biomass and photosynthesis data, both the S3 ( Diaporthe cotoneastri ) and S10 ( Ilyonectria cyclaminicola ) strains promoted the growth of Epimedium koreanum Nakai . Redundancy analysis (RDA) showed that the activity of S3 and the content of epimedin A were negatively correlated and that the peroxidase (POD) activity was positively correlated with the total flavonoid content. Conclusion The application of the S3 ( Diaporthe cotoneastri ) and S10 ( Ilyonectria cyclaminicola ) strains can significantly increase the biomass and contents of total flavonoids, icariin, epimedin B, and epimedin C, but not epimedin A, in Epimedium koreanum Nakai host plants grown in field conditions. The S10 strain promotes faster growth of Epimedium koreanum Nakai than the S3 strain, and flavonoid 3-hydroxylase (F3H) catalyzes the synthesis of epimedin A and icariin by different pathways using the same substrate. POD plays a key role in total flavonoid synthesis in Epimedium koreanum Nakai .
{"title":"Diaporthe cotoneastri and Ilyonectria cyclaminicola endophytes promote the growth, development, and accumulation of active components of Epimedium koreanum Nakai host plants in field experiments","authors":"Jiawen Chen, Xing Hu, Yang Bai, Hanning Liu, Xin Zhuang, Junjie Guo, Jinglei Xiao","doi":"10.1186/s13213-023-01733-8","DOIUrl":"https://doi.org/10.1186/s13213-023-01733-8","url":null,"abstract":"Abstract Purpose This study aims to explore the effects of two endophytes of Epimedium koreanum Nakai on host plant growth and development and medicinal material quality and to promote the growth and development of ingredients derived from Epimedium koreanum Nakai . Methods The effects on the biomass, photosynthesis parameters, chlorophyll fluorescence parameters, activity of key enzymes, and active components in the process of growth and development in Korea were examined. Results From the analysis of biomass and photosynthesis data, both the S3 ( Diaporthe cotoneastri ) and S10 ( Ilyonectria cyclaminicola ) strains promoted the growth of Epimedium koreanum Nakai . Redundancy analysis (RDA) showed that the activity of S3 and the content of epimedin A were negatively correlated and that the peroxidase (POD) activity was positively correlated with the total flavonoid content. Conclusion The application of the S3 ( Diaporthe cotoneastri ) and S10 ( Ilyonectria cyclaminicola ) strains can significantly increase the biomass and contents of total flavonoids, icariin, epimedin B, and epimedin C, but not epimedin A, in Epimedium koreanum Nakai host plants grown in field conditions. The S10 strain promotes faster growth of Epimedium koreanum Nakai than the S3 strain, and flavonoid 3-hydroxylase (F3H) catalyzes the synthesis of epimedin A and icariin by different pathways using the same substrate. POD plays a key role in total flavonoid synthesis in Epimedium koreanum Nakai .","PeriodicalId":8069,"journal":{"name":"Annals of Microbiology","volume":"31 1","pages":"0"},"PeriodicalIF":0.0,"publicationDate":"2023-09-12","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"135827043","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":4,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2023-08-22DOI: 10.1186/s13213-023-01732-9
Jamidah Bagaya, Kenneth Ssekatawa, Gloria Nakabiri, Julius Nsubuga, Anna Kitibwa, Charles Drago Kato, Lawrence Fred Sembajwe
Abstract Background Escherichia coli (E. coli) is one of the most frequent causes of fatal bacterial infections affecting both humans and animals. The resistance to Carbapenems is mainly associated with enzyme-mediated resistance mechanism, through the acquisition of Carbapenemase genes. In Uganda, no studies have been done to detect presence of Carbapenem-resistant E. coli in sewage. We therefore carried out a study to characterize Carbapenem-resistant E. coli from sewage from Mulago National Referral Hospital. Methods and results In this cross-sectional study, a total of 104, sewage samples were aseptically collected, cultured on MacConkey agar supplemented with Meropenem 1 µg/ml with other standard microbiology methods to screen for Carbapenem-resistant E. coli (CREC). Antimicrobial susceptibility testing was performed on the CREC, using Imipenem (10 mg/disc) and Meropenem (10 mg/disc), Carbapenem drugs readily available on market. Multiplex PCR was performed on selected Carbapenem-resistant and susceptible isolates to detect Carbapenemase genes. Later the isolates were pathotyped for virulence genes that included pathogenicity islands (PAIs) and phylogenetic markers. The results showed that the Carbapenem-resistant E. coli isolates were more resistant to Meropenem (64%) than Imipenem (60%). KPC gene was the most predominant (75%), followed by NDM gene (30%) while no OXA-48, IMP-1, and IMP-2 genes were detected. Pathotyping of virulence genes showed presence of eae gene, as the most predominant (40%), followed by elt gene (25%) and negative for stx and aggR genes. For PAI markers, only the PAI IV 536 gene was detected at 10%. Then, pathotyping of the phylogenetic markers was present in 85% of the typed isolates with yjaA gene the most abundant (60%) while both chuA and TSPE4.C2 were detected in 5% of the isolates. Conclusion Both pathogenic and non-pathogenic Carbapenem-resistant E. coli strains are present in the sewage of Mulago National Referral Hospital in Uganda.
摘要背景大肠杆菌是人类和动物最常见的致死性细菌感染之一。对碳青霉烯类的抗性主要与酶介导的抗性机制有关，通过碳青霉烯酶基因的获得。在乌干达，没有进行研究以检测污水中是否存在耐碳青霉烯类大肠杆菌。因此，我们开展了一项研究，以表征来自穆拉戈国家转诊医院污水中的耐碳青霉烯类大肠杆菌。方法与结果本横断面研究共收集104万份污水样本，在添加美罗培南1µg/ml的MacConkey琼脂培养基上进行培养，采用其他标准微生物学方法筛选耐碳青霉烯E. coli (CREC)。采用市售碳青霉烯类药物亚胺培南(10 mg/盘)和美罗培南(10 mg/盘)对CREC进行药敏试验。选择碳青霉烯耐药和敏感菌株进行多重PCR检测碳青霉烯酶基因。随后对毒力基因进行分型，包括致病性岛(PAIs)和系统发育标记。结果表明，耐碳青霉烯大肠杆菌对美罗培南(64%)的耐药率高于亚胺培南(60%)。KPC基因最多(75%)，NDM基因次之(30%)，未检出OXA-48、IMP-1和IMP-2基因。毒力基因的致病分型显示eae基因最多(40%)，其次是elt基因(25%)，stx和aggR基因均阴性。PAI标记物仅PAI IV 536基因检出率为10%。在85%的分型菌株中存在系统发育标记，其中yjaA基因含量最多(60%)，而chuA和TSPE4基因含量都最多。5%的分离株中检出C2。结论乌干达穆拉戈国家转诊医院污水中存在致病性和非致病性碳青霉烯耐药大肠杆菌。
{"title":"Molecular characterization of Carbapenem-resistant Escherichia coli isolates from sewage at Mulago National Referral Hospital, Kampala: a cross-sectional study","authors":"Jamidah Bagaya, Kenneth Ssekatawa, Gloria Nakabiri, Julius Nsubuga, Anna Kitibwa, Charles Drago Kato, Lawrence Fred Sembajwe","doi":"10.1186/s13213-023-01732-9","DOIUrl":"https://doi.org/10.1186/s13213-023-01732-9","url":null,"abstract":"Abstract Background Escherichia coli (E. coli) is one of the most frequent causes of fatal bacterial infections affecting both humans and animals. The resistance to Carbapenems is mainly associated with enzyme-mediated resistance mechanism, through the acquisition of Carbapenemase genes. In Uganda, no studies have been done to detect presence of Carbapenem-resistant E. coli in sewage. We therefore carried out a study to characterize Carbapenem-resistant E. coli from sewage from Mulago National Referral Hospital. Methods and results In this cross-sectional study, a total of 104, sewage samples were aseptically collected, cultured on MacConkey agar supplemented with Meropenem 1 µg/ml with other standard microbiology methods to screen for Carbapenem-resistant E. coli (CREC). Antimicrobial susceptibility testing was performed on the CREC, using Imipenem (10 mg/disc) and Meropenem (10 mg/disc), Carbapenem drugs readily available on market. Multiplex PCR was performed on selected Carbapenem-resistant and susceptible isolates to detect Carbapenemase genes. Later the isolates were pathotyped for virulence genes that included pathogenicity islands (PAIs) and phylogenetic markers. The results showed that the Carbapenem-resistant E. coli isolates were more resistant to Meropenem (64%) than Imipenem (60%). KPC gene was the most predominant (75%), followed by NDM gene (30%) while no OXA-48, IMP-1, and IMP-2 genes were detected. Pathotyping of virulence genes showed presence of eae gene, as the most predominant (40%), followed by elt gene (25%) and negative for stx and aggR genes. For PAI markers, only the PAI IV 536 gene was detected at 10%. Then, pathotyping of the phylogenetic markers was present in 85% of the typed isolates with yjaA gene the most abundant (60%) while both chuA and TSPE4.C2 were detected in 5% of the isolates. Conclusion Both pathogenic and non-pathogenic Carbapenem-resistant E. coli strains are present in the sewage of Mulago National Referral Hospital in Uganda.","PeriodicalId":8069,"journal":{"name":"Annals of Microbiology","volume":"10 1","pages":"0"},"PeriodicalIF":0.0,"publicationDate":"2023-08-22","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"135671050","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":4,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
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