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Pathogens, Volume 11, Issue 5 (May 2022) – 126 articles

Cover Story (view full-size image): Cryptosporidiosis: environmental and human transmission. Soil, water, and unwashed vegetables that are contaminated with oocysts may release them into the environment. Oocysts inhaled by healthcare workers can be spread in nosocomial settings and transmitted from one patient to another. View this paper
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Editorial
New Insights in Acanthamoeba
Pathogens 2022, 11(5), 609; https://0-doi-org.brum.beds.ac.uk/10.3390/pathogens11050609 - 23 May 2022
Viewed by 449
Abstract
Acanthamoeba is a free-living amoeba genus able to cause severe infections, such as Granulomatous amoebic encephalitis (GAE), epithelial disorders and a sight-threatening disease called Acanthamoeba keratitis (AK) [...] Full article
(This article belongs to the Special Issue New Insights in Acanthamoeba)
Article
Investigations on the Efficacy of Ozone as an Environmental Sanitizer in Large Supermarkets
Pathogens 2022, 11(5), 608; https://0-doi-org.brum.beds.ac.uk/10.3390/pathogens11050608 - 23 May 2022
Viewed by 542
Abstract
Awareness of the importance of the microbial contamination of air and surfaces has increased significantly during the COVID-19 pandemic. The aim of this study was to evaluate the presence of bacteria and fungi in the air and on surfaces within some critical areas [...] Read more.
Awareness of the importance of the microbial contamination of air and surfaces has increased significantly during the COVID-19 pandemic. The aim of this study was to evaluate the presence of bacteria and fungi in the air and on surfaces within some critical areas of large supermarkets with and without an ozonation system. Surveys were conducted in four supermarkets belonging to the same commercial chain of an Apulian city in June 2021, of which two (A and B) were equipped with an ozonation system, and two (C and D) did not have any air-diffused remediation treatment. There was a statistically significant difference in the total bacterial count (TBC) and total fungal count (TFC) in the air between A/B and C/D supermarkets (p = 0.0042 and p = 0.0002, respectively). Regarding surfaces, a statistically significant difference in TBC emerged between A/B and C/D supermarkets (p = 0.0101). To the best of our knowledge, this is the first study evaluating the effect of ozone on commercial structures in Italy. Future investigations, supported by a multidisciplinary approach, will make it possible to deepen the knowledge on this method of sanitation, in light of any other epidemic/pandemic waves. Full article
Correction
Correction: Kumar et al. The Global Emergence of Human Babesiosis. Pathogens 2021, 10, 1447
Pathogens 2022, 11(5), 607; https://0-doi-org.brum.beds.ac.uk/10.3390/pathogens11050607 - 23 May 2022
Viewed by 359
Abstract
There were two factual errors in the original publication of our manuscript [...] Full article
Article
Molecular Survey of Vector-Borne Pathogens in Ticks, Sheep Keds, and Domestic Animals from Ngawa, Southwest China
Pathogens 2022, 11(5), 606; https://0-doi-org.brum.beds.ac.uk/10.3390/pathogens11050606 - 22 May 2022
Viewed by 578
Abstract
Vector-borne pathogens are mainly transmitted by blood-feeding arthropods such as ticks, mosquitoes, fleas, lice, mites, etc. They pose a significant threat to animal and human health due to their worldwide distribution. Although much work has been performed on these pathogens, some neglected areas [...] Read more.
Vector-borne pathogens are mainly transmitted by blood-feeding arthropods such as ticks, mosquitoes, fleas, lice, mites, etc. They pose a significant threat to animal and human health due to their worldwide distribution. Although much work has been performed on these pathogens, some neglected areas and undiscovered pathogens are still to be further researched. In this study, ticks (Haemaphysalis qinghaiensis), sheep keds (Melophagus ovinus), and blood samples from yaks and goats were collected in Ngawa Tibetan and Qiang Autonomous Prefecture located on the eastern edge of the Qinghai–Tibet Plateau, Southwest China. Several vector-borne bacterial pathogens were screened and studied. Anaplasma bovis strains representing novel genotypes were detected in ticks (8.83%, 37/419), yak blood samples (45.71%, 64/140), and goat blood samples (58.93%, 33/56). Two spotted fever group (SFG) Rickettsiae, Candidatus Rickettsia jingxinensis, and a novel Rickettsia species named Candidatus Rickettsia hongyuanensis were identified in ticks. Another Rickettsia species closely related to the Rickettsia endosymbiont of Polydesmus complanatus was also detected in ticks. Furthermore, a Coxiella species was detected in ticks (3.34%, 14/419), keds (1.89%, 2/106), and yak blood (0.71%, 1/140). Interestingly, another Coxiella species and a Coxiella-like bacterium were detected in a tick and a goat blood sample, respectively. These results indicate the remarkable diversity of vector-borne pathogens circulating in this area. Further investigations on their pathogenicity to humans and domestic animals are still needed. Full article
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Article
Inhibitor of Cysteine Protease of Plasmodium malariae Regulates Malapains, Endogenous Cysteine Proteases of the Parasite
Pathogens 2022, 11(5), 605; https://0-doi-org.brum.beds.ac.uk/10.3390/pathogens11050605 - 22 May 2022
Viewed by 440
Abstract
Cysteine proteases of malaria parasites have been recognized as potential targets in antimalarial drug development as they play pivotal roles in the biology of these parasites. However, strict regulation of their activities is also necessary to minimize or prevent deleterious damage to the [...] Read more.
Cysteine proteases of malaria parasites have been recognized as potential targets in antimalarial drug development as they play pivotal roles in the biology of these parasites. However, strict regulation of their activities is also necessary to minimize or prevent deleterious damage to the parasite and the host. Previously, we have characterized falcipain family cysteine proteases of Plasmodium malariae, named as malapains (MPs). MPs are active hemoglobinases. They also may participate in the release of merozoites from mature schizonts by facilitating remodeling of erythrocyte skeleton proteins. In this study, we identified and characterized an endogenous inhibitor of cysteine protease of P. malariae (PmICP). PmICP shared similar structural and biochemical properties with ICPs from other Plasmodium species. Recombinant PmICP showed a broad range of inhibitory activities against diverse cysteine proteases such as falcipain family enzymes (MP-2, MP-4, VX-3, VX-4, and FP-3), papain, and human cathepsins B and L, with stronger inhibitory activities against falcipain family enzymes. The inhibitory activity of PmICP was not affected by pH. PmICP was thermo-labile, resulting in rapid loss of its inhibitory activity at a high temperature. PmICP effectively inhibited hemoglobin hydrolysis by MPs and regulated maturation of MPs, suggesting its role as a functional regulator of MPs. Full article
(This article belongs to the Section Parasitic Pathogens)
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Communication
Comparison Study of Four Extraction Methods Combined with PCR and LAMP for Feline Tritrichomonas foetus Detection in Fecal Samples
Pathogens 2022, 11(5), 604; https://0-doi-org.brum.beds.ac.uk/10.3390/pathogens11050604 - 22 May 2022
Viewed by 466
Abstract
Feline trichomonosis occurs worldwide, with gastrointestinal symptoms such as chronic large-bowel diarrhea and abdominal pain. The inclusion of molecular methods in diagnostic and epidemiological studies has necessitated an effective method for extracting DNA from feces. We tested four extraction commercial kits: ZR Fecal [...] Read more.
Feline trichomonosis occurs worldwide, with gastrointestinal symptoms such as chronic large-bowel diarrhea and abdominal pain. The inclusion of molecular methods in diagnostic and epidemiological studies has necessitated an effective method for extracting DNA from feces. We tested four extraction commercial kits: ZR Fecal DNA MiniPrep (50 preps) (Zymo Research, Irvine, CA, USA), QIAamp® DNA Stool Mini Kit (Qiagen Inc., Valencia, CA, USA), UltraClean Fecal DNA Kit (50 preps) (MO BIO, San Diego, CA, USA), and Sherlock AX/100 isolations (A&A Biotechnology, Gdynia, Poland). We assessed the sensitivity of detection of Tritrichomonas foetus in spiked fecal samples for the four kits combined with two molecular assays: PCR and LAMP. The extraction efficacy was quantified using defined aliquots of fecal samples spiked with 5 μL of suspensions containing serial dilutions of trophozoites (0.1; 1; 10; 100; 1000; 10,000), with six replicates for each concentration. In our study, we proved that the ZR Fecal DNA MiniPrep (50 preps) kit combined with LAMP and PCR had the highest efficiency among all the compared methods for the detection of feline T. foetus from fecal samples. Full article
(This article belongs to the Topic Host–Parasite Interactions)
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Article
Prevalence of Toxoplasma gondii Antibodies in Individuals Occupationally Exposed to Livestock in Portugal
Pathogens 2022, 11(5), 603; https://0-doi-org.brum.beds.ac.uk/10.3390/pathogens11050603 - 22 May 2022
Viewed by 597
Abstract
Toxoplasmosis is a worldwide zoonotic disease with different and complex routes for transmission. Workers occupationally exposed to animals or raw meat and viscera (WOE) may be at more risk than the general population, however conflicting data exist on the risk of developing toxoplasmosis [...] Read more.
Toxoplasmosis is a worldwide zoonotic disease with different and complex routes for transmission. Workers occupationally exposed to animals or raw meat and viscera (WOE) may be at more risk than the general population, however conflicting data exist on the risk of developing toxoplasmosis due to this close contact. To add knowledge to this topic, the aim of the present study was to ascertain if WOE were more likely to be anti-T. gondii IgG seropositive than the general population as well as to study risk factors for T. gondii infection such as professional activity, gender, age, years of work and region. For this purpose, a case–control study using archived samples was setup. A total of 114 WOE (including pig slaughterhouse workers, butchers, veterinarians and farmers) and 228 anonymous volunteers (matched with cases by region, age and gender) were studied for anti-T. gondii IgG. A significantly higher anti-T. gondii IgG occurrence (p = 0.0282) was found in WOE when compared with the general population (72.8% [CI = 64.6–81.0%] versus 60.1% [CI = 54.6–65.6%]). Multivariate analysis showed that WOE of more than 50 years of age were more likely to be seropositive for anti-T. gondii IgG (aOR = 16.8; 95% CI 3.6–77.5; p < 0.001) than those aged less than 50 years. To our knowledge, this is the first case–control study on the prevalence of anti-T. gondii IgG in WOE in Portugal, also showing an added risk for T. gondii infection in those exposed to animals or their meat and viscera. Full article
(This article belongs to the Special Issue Advanced Research on Foodborne Pathogens)
Article
Redirecting Imipramine against Bluetongue Virus Infection: Insights from a Genome-wide Haploid Screening Study
Pathogens 2022, 11(5), 602; https://0-doi-org.brum.beds.ac.uk/10.3390/pathogens11050602 - 22 May 2022
Viewed by 566
Abstract
Bluetongue virus (BTV), an arbovirus of ruminants, is a causative agent of numerous epidemics around the world. Due to the emergence of novel reassortant BTV strains and new outbreaks, there is an unmet need for efficacious antivirals. In this study, we used an [...] Read more.
Bluetongue virus (BTV), an arbovirus of ruminants, is a causative agent of numerous epidemics around the world. Due to the emergence of novel reassortant BTV strains and new outbreaks, there is an unmet need for efficacious antivirals. In this study, we used an improved haploid screening platform to identify the relevant host factors for BTV infection. Our screening tool identified and validated the host factor Niemann–Pick C1 (NPC1), a lysosomal membrane protein that is involved in lysosomal cholesterol transport, as a critical factor in BTV infection. This finding prompted us to investigate the possibility of testing imipramine, an antidepressant drug known to inhibit NPC1 function by interfering with intracellular cholesterol trafficking. In this study, we evaluated the sensitivity of BTV to imipramine using in vitro assays. Our results demonstrate that imipramine pretreatment inhibited in vitro replication and progeny release of BTV-4, BTV-8, and BTV-16. Collectively, our findings highlight the importance of NPC1 for BTV infection and recommend the reprofiling of imipramine as a potential antiviral drug against BTV. Full article
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Article
Comparative Whole Genome Analysis of an Anaplasma phagocytophilum Strain Isolated from Norwegian Sheep
Pathogens 2022, 11(5), 601; https://0-doi-org.brum.beds.ac.uk/10.3390/pathogens11050601 - 21 May 2022
Viewed by 585
Abstract
Anaplasma phagocytophilum is a Gram-negative obligate intracellular tick-borne alphaproteobacteria (family Anaplasmatacea, order Rickettsiales) with a worldwide distribution. In Norway, tick borne fever (TBF), caused by A. phagocytophilum, presents a major challenge in sheep farming. Despite the abundance of its tick vector, Ixodes [...] Read more.
Anaplasma phagocytophilum is a Gram-negative obligate intracellular tick-borne alphaproteobacteria (family Anaplasmatacea, order Rickettsiales) with a worldwide distribution. In Norway, tick borne fever (TBF), caused by A. phagocytophilum, presents a major challenge in sheep farming. Despite the abundance of its tick vector, Ixodes ricinus, and A. phagocytophilum infections in wild and domestic animals, reports of infections in humans are low compared with cases in the U.S. Although A. phagocytophilum is genetically diverse and complex infections (co-infection and superinfection) in ruminants and other animals are common, the underlying genetic basis of intra-species interactions and host-specificity remains unexplored. Here, we performed whole genome comparative analysis of a newly cultured Norwegian A. phagocytophilum isolate from sheep (ApSheep_NorV1) with 27 other A. phagocytophilum genome sequences derived from human and animal infections worldwide. Although the compared strains are syntenic, there is remarkable genetic diversity between different genomic loci including the pfam01617 superfamily that encodes the major, neutralization-sensitive, surface antigen Msp2/p44. Blast comparisons between the msp2/p44 pseudogene repertoires from all the strains showed high divergence between U. S. and European strains and even between two Norwegian strains. Based on these comparisons, we concluded that in ruminants, complex infections can be attributed to infection with strains that differ in their msp2/p44 repertoires, which has important implications for pathogen evolution and vaccine development. We also present evidence for integration of rickettsial DNA into the genome of ISE6 tick cells. Full article
(This article belongs to the Special Issue Emerging Infections in Small Ruminants)
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Article
The Influence of Contracaecum larvae (Nematoda, Anisakidae) Parasitism on the Population of Prussian carp (Carassius gibelio) in Lake Sakadaš, Croatia
Pathogens 2022, 11(5), 600; https://0-doi-org.brum.beds.ac.uk/10.3390/pathogens11050600 - 21 May 2022
Viewed by 493
Abstract
Contracaecum larvae are geographically widely distributed, utilizing many animal species as hosts; and fish represent an important paratenic host in their life cycle. Their presence in Prussian carp (Carassius gibelio) was studied in Lake Sakadaš (Croatia) in 2017 and 2018. Two [...] Read more.
Contracaecum larvae are geographically widely distributed, utilizing many animal species as hosts; and fish represent an important paratenic host in their life cycle. Their presence in Prussian carp (Carassius gibelio) was studied in Lake Sakadaš (Croatia) in 2017 and 2018. Two gill nets of different sizes submerged during a 12-h period were used to collect the fish. Contracaecum larvae were recorded in the stomach, slightly coiled or elongated on the intestine serosa or encapsulated in a gut wall of 20 individuals. The effect of Contracaecum sp. on the health of their host was determined by estimating the effect of the parasites’ presence, number, and biomass on fish length, weight, and the Fulton’s condition factor (CF). Infected fish showed negative (b < 3; p < 0.05) and uninfected fish positive allometric growth (b > 3; p < 0.05). Fish weight and CF in infected individuals were significantly low in comparison to the uninfected ones (Mann–Whitney U test: U = 1078.00, U = 423.50, respectively; p < 0.004). These results emphasize the importance of evaluating parasitic nematode presence in economically important fish species. Even more, if this endoparasite has a detectable negative impact on a resilient species such as the Prussian carp, it is important to monitor its occurrence in other fish species. Full article
(This article belongs to the Special Issue Anisakiasis and Anisakidae)
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Article
An Alternative Culture Medium for Continuous In Vitro Propagation of the Human Pathogen Babesia duncani in Human Erythrocytes
Pathogens 2022, 11(5), 599; https://0-doi-org.brum.beds.ac.uk/10.3390/pathogens11050599 - 20 May 2022
Viewed by 556
Abstract
Continuous propagation of Babesia duncani in vitro in human erythrocytes and the availability of a mouse model of B. duncani lethal infection make this parasite an ideal model to study Babesia biology and pathogenesis. Two culture media, HL-1 and Claycomb, with proprietary formulations [...] Read more.
Continuous propagation of Babesia duncani in vitro in human erythrocytes and the availability of a mouse model of B. duncani lethal infection make this parasite an ideal model to study Babesia biology and pathogenesis. Two culture media, HL-1 and Claycomb, with proprietary formulations are the only culture media known to support the parasite growth in human erythrocytes; however, the HL-1 medium has been discontinued and the Claycomb medium is often unavailable leading to major interruptions in the study of this pathogen. To identify alternative media conditions, we evaluated the growth of B. duncani in various culture media with well-defined compositions. We report that the DMEM-F12 culture medium supports the continuous growth of the parasite in human erythrocytes to levels equal to those achieved in the HL-1 and Claycomb media. We generated new clones of B. duncani from the parental WA-1 clinical isolate after three consecutive subcloning events in this medium. All clones showed a multiplication rate in vitro similar to that of the WA-1 parental isolate and cause fatal infection in C3H/HeJ mice. The culture medium, which can be readily reconstituted from its individual components, and the tools and resources developed here will facilitate the study of B. duncani. Full article
(This article belongs to the Special Issue Babesia and Human Babesiosis)
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Case Report
Pericardial Effusion Due to Trichosporon japonicum: A Case Report and Review of the Literature
Pathogens 2022, 11(5), 598; https://0-doi-org.brum.beds.ac.uk/10.3390/pathogens11050598 - 20 May 2022
Viewed by 430
Abstract
Invasive infections due to Trichosporon spp. are life-threatening opportunistic fungal infections that may affect a wide array of organs. Here, we described a case of pericardial effusion due to Trichosporon japonicum in a 42-year-old female after a heart transplantation. T. japonicum was [...] Read more.
Invasive infections due to Trichosporon spp. are life-threatening opportunistic fungal infections that may affect a wide array of organs. Here, we described a case of pericardial effusion due to Trichosporon japonicum in a 42-year-old female after a heart transplantation. T. japonicum was isolated from the pericardial fluid, pericardial drain hole and the swab of the sternal surgery scar wound. The late mycological diagnosis due to blood culture negative, the ineffective control of pulmonary bacterial infection and the late start antifungal therapy were the contributing factors in the patient’s death. Full article
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Article
Experimental Bovine Spongiform Encephalopathy in Squirrel Monkeys: The Same Complex Proteinopathy Appearing after Very Different Incubation Times
Pathogens 2022, 11(5), 597; https://0-doi-org.brum.beds.ac.uk/10.3390/pathogens11050597 - 20 May 2022
Viewed by 627
Abstract
Incubation periods in humans infected with transmissible spongiform encephalopathy (TSE) agents can exceed 50 years. In humans infected with bovine spongiform encephalopathy (BSE) agents, the effects of a “species barrier,” often observed when TSE infections are transmitted from one species to another, would [...] Read more.
Incubation periods in humans infected with transmissible spongiform encephalopathy (TSE) agents can exceed 50 years. In humans infected with bovine spongiform encephalopathy (BSE) agents, the effects of a “species barrier,” often observed when TSE infections are transmitted from one species to another, would be expected to increase incubation periods compared with transmissions of same infectious agents within the same species. As part of a long-term study investigating the susceptibility to BSE of cell cultures used to produce vaccines, we inoculated squirrel monkeys (Saimiri sp., here designated SQ) with serial dilutions of a bovine brain suspension containing the BSE agent and monitored them for as long as ten years. Previously, we showed that SQ infected with the original “classical” BSE agent (SQ-BSE) developed a neurological disease resembling that seen in humans with variant CJD (vCJD). Here, we report the final characterization of the SQ-BSE model. We observed an unexpectedly marked difference in incubation times between two animals inoculated with the same dilution and volume of the same C-BSE bovine brain extract on the same day. SQ-BSE developed, in addition to spongiform changes and astrogliosis typical of TSEs, a complex proteinopathy with severe accumulations of protease-resistant prion protein (PrPTSE), hyperphosphorylated tau (p-tau), ubiquitin, and α-synuclein, but without any amyloid plaques or β-amyloid protein (Aβ) typical of Alzheimer’s disease. These results suggest that PrPTSE enhanced the accumulation of several key proteins characteristically seen in human neurodegenerative diseases. The marked variation in incubation periods in the same experimental TSE should be taken into account when modeling the epidemiology of human TSEs. Full article
(This article belongs to the Special Issue Human Prion Disease)
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Article
Cobalt (II) Chloride Regulates the Invasion and Survival of Brucella abortus 544 in RAW 264.7 Cells and B6 Mice
Pathogens 2022, 11(5), 596; https://0-doi-org.brum.beds.ac.uk/10.3390/pathogens11050596 - 18 May 2022
Viewed by 506
Abstract
The effects of Cobalt (II) chloride (CoCl2) in the context of Brucella abortus (B. abortus) infection have not been evaluated so far. Firstly, we found that CoCl2 treatment inhibited the phagocytosis of B. abortus into RAW 264.7 cells. [...] Read more.
The effects of Cobalt (II) chloride (CoCl2) in the context of Brucella abortus (B. abortus) infection have not been evaluated so far. Firstly, we found that CoCl2 treatment inhibited the phagocytosis of B. abortus into RAW 264.7 cells. The inhibition of bacterial invasion was regulated by F-actin formation and associated with a reduction in the phosphorylation of ERK1/2 and HIF-1α expression. Secondly, the activation of trafficking regulators LAMP1, LAMP2, and lysosomal enzyme GLA at the transcriptional level activated immune responses, weakening the B. abortus growth at 4 h post-infection (pi). The silencing of HIF-1α increased bacterial survival at 24 h pi. At the same time, CoCl2 treatment showed a significant increase in the transcripts of lysosomal enzyme HEXB and cytokine TNF-α and an attenuation of the bacterial survival. Moreover, the enhancement at the protein level of HIF-1α was induced in the CoCl2 treatment at both 4 and 24 h pi. Finally, our results demonstrated that CoCl2 administration induced the production of serum cytokines IFN-γ and IL-6, which is accompanied by dampened Brucella proliferation in the spleen and liver of treated mice, and reduced the splenomegaly and hepatomegaly. Altogether, CoCl2 treatment contributed to host resistance against B. abortus infection with immunomodulatory effects. Full article
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Article
Biocontrol of Wheat Crown Rot Using Bacillus halotolerans QTH8
Pathogens 2022, 11(5), 595; https://0-doi-org.brum.beds.ac.uk/10.3390/pathogens11050595 - 18 May 2022
Viewed by 547
Abstract
Fusarium pseudograminearum causes crown rot in wheat. This study aimed to assess the effects of the bacterial strain QTH8 isolated from Cotinus coggygria rhizosphere soil against F. pseudograminearum. Bacterial strain QTH8 was identified as Bacillus halotolerans in accordance with the phenotypic traits [...] Read more.
Fusarium pseudograminearum causes crown rot in wheat. This study aimed to assess the effects of the bacterial strain QTH8 isolated from Cotinus coggygria rhizosphere soil against F. pseudograminearum. Bacterial strain QTH8 was identified as Bacillus halotolerans in accordance with the phenotypic traits and the phylogenetic analysis of 16S rDNA and gyrB gene sequence. Culture filtrates of bacterial strain QTH8 inhibited the mycelial growth of F. pseudograminearum and resulted in mycelial malformation such as tumor formation, protoplast condensation, and mycelial fracture. In addition, bacterial strain QTH8 also inhibited the mycelial growth of Hainesia lythri, Pestalotiopsis sp., Botrytis cinerea, Curvularia lunata, Phyllosticta theaefolia, Fusarium graminearum, Phytophthora nicotianae, and Sclerotinia sclerotiorum. The active compounds produced by bacterial strain QTH8 were resistant to pH, ultraviolet irradiation, and low temperature, and were relatively sensitive to high temperature. After 4 h exposure, culture filtrates of bacterial strain QTH8—when applied at 5%, 10%, 15%, 20%, 25%, and 30%—significantly reduced conidial germination of F. pseudograminearum. The coleoptile infection assay proved that bacterial strain QTH8 reduced the disease index of wheat crown rot. In vivo application of QTH8 to wheat seedlings decreased the disease index of wheat crown rot and increased root length, plant height, and fresh weight. Iturin, surfactin, and fengycin were detected in the culture extract of bacterial strain QTH8 by matrix-assisted laser desorption ionization time-of-flight mass spectrometry (MALDI-TOF-MS). Bacterial strain QTH8 was identified for the presence of the ituC, bacA, bmyB, spaS, srfAB, fend, and srfAA genes using the specific polymerase chain reaction primers. B. halotolerans QTH8 has a vital potential for the sustainable biocontrol of wheat crown rot. Full article
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Communication
Multiplex TaqMan® Quantitative PCR Assays for Host-Tick-Pathogen Studies Using the Guinea Pig-Tick-Rickettsia System
Pathogens 2022, 11(5), 594; https://0-doi-org.brum.beds.ac.uk/10.3390/pathogens11050594 - 18 May 2022
Viewed by 494
Abstract
Spotted Fever Rickettsiosis (SFR) is caused by spotted fever group Rickettsia spp. (SFGR), and is associated with symptoms common to other illnesses, making it challenging to diagnose before detecting SFGR-specific antibodies. The guinea pig is a valuable biomedical model for studying Spotted Fever [...] Read more.
Spotted Fever Rickettsiosis (SFR) is caused by spotted fever group Rickettsia spp. (SFGR), and is associated with symptoms common to other illnesses, making it challenging to diagnose before detecting SFGR-specific antibodies. The guinea pig is a valuable biomedical model for studying Spotted Fever Rickettsiosis (SFR); its immune system is more like the human immune system than that of the murine model, and guinea pigs develop characteristic clinical signs. Thus, we have a compelling interest in developing, expanding, and optimizing tools for use in our guinea pig-Amblyomma-Rickettsia system for understanding host-tick-pathogen interactions. With the design and optimization of the three multiplex TaqMan® qPCR assays described here, we can detect the two SFGR, their respective primary Amblyomma sp. vectors, and the guinea pig model as part of controlled experimental studies using tick-transmission of SFGR to guinea pigs. We developed qPCR assays that reliably detect each specific target down to 10 copies by producing plasmid standards for each assay target, optimizing the individual primer-probe sets, and optimizing the final multiplex reactions in a methodical, stepwise fashion. We anticipate that these assays, currently designed for in vivo studies, will serve as a foundation for optimal SFGR detection in other systems, including fieldwork. Full article
(This article belongs to the Special Issue Understanding Host-Tick-Pathogen Interactions through Animal Models)
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Article
Hagnosa longicapillata, gen. nov., sp. nov., a New Sordariaceous Ascomycete in the Indoor Environment, and the Proposal of Hagnosaceae fam. nov.
Pathogens 2022, 11(5), 593; https://0-doi-org.brum.beds.ac.uk/10.3390/pathogens11050593 - 18 May 2022
Viewed by 622
Abstract
Hagnosa longicapillata, gen. nov., sp. nov, is described and illustrated from wooden building materials collected in Hungary and from pure culture. This species has been collected exclusively from indoor environments, where it was quite common. The ascocarps develop in a thick layer [...] Read more.
Hagnosa longicapillata, gen. nov., sp. nov, is described and illustrated from wooden building materials collected in Hungary and from pure culture. This species has been collected exclusively from indoor environments, where it was quite common. The ascocarps develop in a thick layer of brown, woolly mats of mycelia. The ostiolar region of the perithecia is ornamented with a five-lobed, flower-shaped crown. Asci are four-spored; ascospores are dark brown, smooth, muriform, not constricted at the septa, and liberated mostly through crackings of the thin ascomatal wall. Apparently, ascospores are dispersed by the mechanical disturbance of the mycelial web. In the phylogenetic tree, Hagnosa samples were placed as a basal lineage, independently from the other family of Sordariomycetidae, with high support. To place Hagnosa in Sordariales, the new family, Hagnosaceae, is proposed. Full article
(This article belongs to the Special Issue Detection of Indoor Fungi)
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Article
Microbial Contamination of Preservative-Free Artificial Tears Based on Instillation Techniques
Pathogens 2022, 11(5), 592; https://0-doi-org.brum.beds.ac.uk/10.3390/pathogens11050592 - 18 May 2022
Viewed by 441
Abstract
Preservative-free artificial tears eliminate the side effects of preservatives but are prone to microbial contamination. This study evaluates the incidence of microbial contaminations in single-use vials of preservative-free 0.1% hyaluronate artificial tears. Based on what touched the vial tip during its first use, [...] Read more.
Preservative-free artificial tears eliminate the side effects of preservatives but are prone to microbial contamination. This study evaluates the incidence of microbial contaminations in single-use vials of preservative-free 0.1% hyaluronate artificial tears. Based on what touched the vial tip during its first use, 60 unit-dose vials (0.5 mL) were divided into groups A (no touch, n = 20), B (fingertip, n = 20), and C (lid margin, n = 20). The vials were recapped after the first use, and the residual solution was cultured 24 h later. The solution from 20 aseptically opened and unused vials was also cultured (group D). Microbial contamination rates were compared between the groups using the Fisher’s exact test. Groups B and C contained 45% (9/20) and 10% (2/20) contaminations while groups A and D contained undetected microbial growth. The culture positivity rates were significantly different between groups A and B (p = 0.001) and groups B and C (p = 0.013) but not between groups A and C (p = 0.487). We demonstrate a significantly higher risk of contamination when fingertips touch the vial mouth. Therefore, users should avoid the vial tip touching the fingers or eyelid during instillation to prevent contamination of the eye drops. Full article
(This article belongs to the Special Issue Microorganisms Living in the Skin)
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Article
The GP-45 Protein, a Highly Variable Antigen from Babesia bigemina, Contains Conserved B-Cell Epitopes in Geographically Distant Isolates
Pathogens 2022, 11(5), 591; https://0-doi-org.brum.beds.ac.uk/10.3390/pathogens11050591 - 18 May 2022
Viewed by 709
Abstract
In B. bigemina, the 45 kilodaltons glycoprotein (GP-45) is the most studied. GP-45 is exposed on the surface of the B. bigemina merozoite, it is believed to play a role in the invasion of erythrocytes, and it is characterized by a high [...] Read more.
In B. bigemina, the 45 kilodaltons glycoprotein (GP-45) is the most studied. GP-45 is exposed on the surface of the B. bigemina merozoite, it is believed to play a role in the invasion of erythrocytes, and it is characterized by a high genetic and antigenic polymorphism. The objective of this study was to determine if GP-45 contains conserved B-cell epitopes, and if they would induce neutralizing antibodies. The comparative analysis of nucleotide and amino acids sequences revealed a high percentage of similarity between field isolates. Antibodies against peptides containing conserved B-cell epitopes of GP-45 were generated. Antibodies present in the sera of mice immunized with GP-45 peptides specifically recognize B. bigemina by the IFAT. More than 95% of cattle naturally infected with B. bigemina contained antibodies against conserved GP-45 peptides tested by ELISA. Finally, sera from rabbits immunized with GP-45 peptides were evaluated in vitro neutralization tests and it was shown that they reduced the percentage of parasitemia compared to sera from rabbits immunized with adjuvant. GP-45 from geographically distant isolates of B. bigemina contains conserved B-cell epitopes that induce neutralizing antibodies suggesting that this gene and its product play a critical role in the survival of the parasite under field conditions. Full article
(This article belongs to the Special Issue Advances in the Epidemiological Surveillance of Tick-Borne Pathogens)
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Article
Proteomic Characterization of the Oral Pathogen Filifactor alocis Reveals Key Inter-Protein Interactions of Its RTX Toxin: FtxA
Pathogens 2022, 11(5), 590; https://0-doi-org.brum.beds.ac.uk/10.3390/pathogens11050590 - 17 May 2022
Viewed by 602
Abstract
Filifactor alocis is a Gram-positive asaccharolytic, obligate anaerobic rod that has been isolated from a variety of oral infections including periodontitis, peri-implantitis, and odontogenic abscesses. As a newly emerging pathogen, its type strain has been investigated for pathogenic properties, yet little is known [...] Read more.
Filifactor alocis is a Gram-positive asaccharolytic, obligate anaerobic rod that has been isolated from a variety of oral infections including periodontitis, peri-implantitis, and odontogenic abscesses. As a newly emerging pathogen, its type strain has been investigated for pathogenic properties, yet little is known about its virulence variations among strains. We previously screened the whole genome of nine clinical oral isolates and a reference strain of F. alocis, and they expressed a novel RTX toxin, FtxA. In the present study, we aimed to use label-free quantification proteomics to characterize the full proteome of those ten F. alocis strains. A total of 872 proteins were quantified, and 97 among them were differentially expressed in FtxA-positive strains compared with the negative strains. In addition, 44 of these differentially expressed proteins formed 66 pairs of associations based on their predicted functions, which included clusters of proteins with DNA repair/mediated transformation and catalytic activity-related function, indicating different biosynthetic activities among strains. FtxA displayed specific interactions with another six intracellular proteins, forming a functional cluster that could discriminate between FtxA-producing and non-producing strains. Among them were FtxB and FtxD, predicted to be encoded by the same operon as FtxA. While revealing the broader qualitative and quantitative proteomic landscape of F. alocis, this study also sheds light on the deeper functional inter-relationships of FtxA, thus placing this RTX family member into context as a major virulence factor of this species. Full article
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Article
Significance of Mucosa-Associated Microbiota and Its Impacts on Intestinal Health of Pigs Challenged with F18+ E. coli
Pathogens 2022, 11(5), 589; https://0-doi-org.brum.beds.ac.uk/10.3390/pathogens11050589 - 17 May 2022
Viewed by 571
Abstract
The objective of this study was to evaluate the significance of jejunal mucosa-associated microbiota and its impacts on the intestinal health of pigs challenged with F18+ Escherichia coli. Forty-four newly-weaned pigs were allotted to two treatments in a randomized complete [...] Read more.
The objective of this study was to evaluate the significance of jejunal mucosa-associated microbiota and its impacts on the intestinal health of pigs challenged with F18+ Escherichia coli. Forty-four newly-weaned pigs were allotted to two treatments in a randomized complete block design with sex as blocks. Pigs were fed common diets for 28 d. At d 7 post-weaning, pigs were orally inoculated with saline solution or F18+ E. coli. At d 21 post-challenge, feces and blood were collected and pigs were euthanized to collect jejunal tissue to evaluate microbiota and intestinal health parameters. The relative abundance of Firmicutes and Bacteroidetes was lower (p < 0.05) in jejunal mucosa than in feces, whereas Proteobacteria was greater (p < 0.05) in jejunal mucosa. F18+ E. coli increased (p < 0.05) protein carbonyl, Helicobacteraceae, Pseudomonadaceae, Xanthomonadaceae, and Peptostreptococcaceae and reduced (p < 0.05) villus height, Enterobacteriaceae, Campylobacteraceae, Brachyspiraceae, and Caulobacteraceae in jejunal mucosa, whereas it reduced (p < 0.05) Spirochaetaceae and Oscillospiraceae in feces. Collectively, jejunal mucosa-associated microbiota differed from those in feces. Compared with fecal microbiota, the change of mucosa-associated microbiota by F18+ E. coli was more prominent, and it was mainly correlated with increased protein carbonyl and reduced villus height in jejunal mucosa impairing the intestinal health of nursery pigs. Full article
(This article belongs to the Special Issue Modulation of Gut Microbiota & Microbiome in Pigs)
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Article
Virus-Derived Chemokine Modulating Protein Pre-Treatment Blocks Chemokine–Glycosaminoglycan Interactions and Significantly Reduces Transplant Immune Damage
Pathogens 2022, 11(5), 588; https://0-doi-org.brum.beds.ac.uk/10.3390/pathogens11050588 - 16 May 2022
Viewed by 563
Abstract
Immune cell invasion after the transplantation of solid organs is directed by chemokines binding to glycosaminoglycans (GAGs), creating gradients that guide immune cell infiltration. Renal transplant is the preferred treatment for end stage renal failure, but organ supply is limited and allografts are [...] Read more.
Immune cell invasion after the transplantation of solid organs is directed by chemokines binding to glycosaminoglycans (GAGs), creating gradients that guide immune cell infiltration. Renal transplant is the preferred treatment for end stage renal failure, but organ supply is limited and allografts are often injured during transport, surgery or by cytokine storm in deceased donors. While treatment for adaptive immune responses during rejection is excellent, treatment for early inflammatory damage is less effective. Viruses have developed highly active chemokine inhibitors as a means to evade host responses. The myxoma virus-derived M-T7 protein blocks chemokine: GAG binding. We have investigated M-T7 and also antisense (ASO) as pre-treatments to modify chemokine: GAG interactions to reduce donor organ damage. Immediate pre-treatment of donor kidneys with M-T7 to block chemokine: GAG binding significantly reduced the inflammation and scarring in subcapsular and subcutaneous allografts. Antisense to N-deacetylase N-sulfotransferase1 (ASONdst1) that modifies heparan sulfate, was less effective with immediate pre-treatment, but reduced scarring and C4d staining with donor pre-treatment for 7 days before transplantation. Grafts with conditional Ndst1 deficiency had reduced inflammation. Local inhibition of chemokine: GAG binding in donor organs immediately prior to transplant provides a new approach to reduce transplant damage and graft loss. Full article
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Review
Scratching the Itch: Updated Perspectives on the Schistosomes Responsible for Swimmer’s Itch around the World
Pathogens 2022, 11(5), 587; https://0-doi-org.brum.beds.ac.uk/10.3390/pathogens11050587 - 16 May 2022
Cited by 1 | Viewed by 577
Abstract
Although most studies of digenetic trematodes of the family Schistosomatidae dwell on representatives causing human schistosomiasis, the majority of the 130 identified species of schistosomes infect birds or non-human mammals. The cercariae of many of these species can cause swimmer’s itch when they [...] Read more.
Although most studies of digenetic trematodes of the family Schistosomatidae dwell on representatives causing human schistosomiasis, the majority of the 130 identified species of schistosomes infect birds or non-human mammals. The cercariae of many of these species can cause swimmer’s itch when they penetrate human skin. Recent years have witnessed a dramatic increase in our understanding of schistosome diversity, now encompassing 17 genera with eight more lineages awaiting description. Collectively, schistosomes exploit 16 families of caenogastropod or heterobranch gastropod intermediate hosts. Basal lineages today are found in marine gastropods and birds, but subsequent diversification has largely taken place in freshwater, with some reversions to marine habitats. It seems increasingly likely that schistosomes have on two separate occasions colonized mammals. Swimmer’s itch is a complex zoonotic disease manifested through several different routes of transmission involving a diversity of different host species. Swimmer’s itch also exemplifies the value of adopting the One Health perspective in understanding disease transmission and abundance because the schistosomes involved have complex life cycles that interface with numerous species and abiotic components of their aquatic environments. Given the progress made in revealing their diversity and biology, and the wealth of questions posed by itch-causing schistosomes, they provide excellent models for implementation of long-term interdisciplinary studies focused on issues pertinent to disease ecology, the One Health paradigm, and the impacts of climate change, biological invasions and other environmental perturbations. Full article
(This article belongs to the Special Issue Advances in Avian Schistosomes and Cercarial Dermatitis)
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Article
Discrimination of Methicillin-resistant Staphylococcus aureus by MALDI-TOF Mass Spectrometry with Machine Learning Techniques in Patients with Staphylococcus aureus Bacteremia
Pathogens 2022, 11(5), 586; https://0-doi-org.brum.beds.ac.uk/10.3390/pathogens11050586 - 16 May 2022
Viewed by 547
Abstract
Early administration of proper antibiotics is considered to improve the clinical outcomes of Staphylococcus aureus bacteremia (SAB), but routine clinical antimicrobial susceptibility testing takes an additional 24 h after species identification. Recent studies elucidated matrix-assisted laser desorption/ionization time-of-flight mass spectra to discriminate methicillin-resistant [...] Read more.
Early administration of proper antibiotics is considered to improve the clinical outcomes of Staphylococcus aureus bacteremia (SAB), but routine clinical antimicrobial susceptibility testing takes an additional 24 h after species identification. Recent studies elucidated matrix-assisted laser desorption/ionization time-of-flight mass spectra to discriminate methicillin-resistant strains (MRSA) or even incorporated with machine learning (ML) techniques. However, no universally applicable mass peaks were revealed, which means that the discrimination model might need to be established or calibrated by local strains’ data. Here, a clinically feasible workflow was provided. We collected mass spectra from SAB patients over an 8-month duration and preprocessed by binning with reference peaks. Machine learning models were trained and tested by samples independently of the first six months and the following two months, respectively. The ML models were optimized by genetic algorithm (GA). The accuracy, sensitivity, specificity, and AUC of the independent testing of the best model, i.e., SVM, under the optimal parameters were 87%, 75%, 95%, and 87%, respectively. In summary, almost all resistant results were truly resistant, implying that physicians might escalate antibiotics for MRSA 24 h earlier. This report presents an attainable method for clinical laboratories to build an MRSA model and boost the performance using their local data. Full article
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Review
Hemoglobin Endocytosis and Intracellular Trafficking: A Novel Way of Heme Acquisition by Leishmania
Pathogens 2022, 11(5), 585; https://0-doi-org.brum.beds.ac.uk/10.3390/pathogens11050585 - 16 May 2022
Viewed by 610
Abstract
Leishmania species are causative agents of human leishmaniasis, affecting 12 million people annually. Drugs available for leishmaniasis are toxic, and no vaccine is available. Thus, the major thrust is to identify new therapeutic targets. Leishmania is an auxotroph for heme and must acquire [...] Read more.
Leishmania species are causative agents of human leishmaniasis, affecting 12 million people annually. Drugs available for leishmaniasis are toxic, and no vaccine is available. Thus, the major thrust is to identify new therapeutic targets. Leishmania is an auxotroph for heme and must acquire heme from the host for its survival. Thus, the major focus has been to understand the heme acquisition process by the parasites in the last few decades. It is conceivable that the parasite is possibly obtaining heme from host hemoprotein, as free heme is not available in the host. Current understanding indicates that Leishmania internalizes hemoglobin (Hb) through a specific receptor by a clathrin-mediated endocytic process and targets it to the parasite lysosomes via the Rab5 and Rab7 regulated endocytic pathway, where it is degraded to generate intracellular heme that is used by the parasite. Subsequently, intra-lysosomal heme is initially transported to the cytosol and is finally delivered to the mitochondria via different heme transporters. Studies using different null mutant parasites showed that these receptors and transporters are essential for the survival of the parasite. Thus, the heme acquisition process in Leishmania may be exploited for the development of novel therapeutics. Full article
(This article belongs to the Special Issue Frontiers in Leishmania)
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Review
The Microbiome as Part of the Contemporary View of Tuberculosis Disease
Pathogens 2022, 11(5), 584; https://0-doi-org.brum.beds.ac.uk/10.3390/pathogens11050584 - 16 May 2022
Viewed by 603
Abstract
The study of the microbiome has changed our overall perspective on health and disease. Although studies of the lung microbiome have lagged behind those on the gastrointestinal microbiome, there is now evidence that the lung microbiome is a rich, dynamic ecosystem. Tuberculosis is [...] Read more.
The study of the microbiome has changed our overall perspective on health and disease. Although studies of the lung microbiome have lagged behind those on the gastrointestinal microbiome, there is now evidence that the lung microbiome is a rich, dynamic ecosystem. Tuberculosis is one of the oldest human diseases, it is primarily a respiratory infectious disease caused by strains from the Mycobacterium tuberculosis Complex. Even today, during the COVID-19 pandemic, it remains one of the principal causes of morbidity and mortality worldwide. Tuberculosis disease manifests itself as a dynamic spectrum that ranges from asymptomatic latent infection to life-threatening active disease. The review aims to provide an overview of the microbiome in the tuberculosis setting, both in patients’ and animal models. We discuss the relevance of the microbiome and its dysbiosis, and how, probably through its interaction with the immune system, it is a significant factor in tuberculosis’s susceptibility, establishment, and severity. Full article
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Article
Comparative Analysis of Structural Features in SLiMs from Eukaryotes, Bacteria, and Viruses with Importance for Host-Pathogen Interactions
Pathogens 2022, 11(5), 583; https://0-doi-org.brum.beds.ac.uk/10.3390/pathogens11050583 - 15 May 2022
Viewed by 548
Abstract
Protein-protein interactions drive functions in eukaryotes that can be described by short linear motifs (SLiMs). Conservation of SLiMs help illuminate functional SLiMs in eukaryotic protein families. However, the simplicity of eukaryotic SLiMs makes them appear by chance due to mutational processes not only [...] Read more.
Protein-protein interactions drive functions in eukaryotes that can be described by short linear motifs (SLiMs). Conservation of SLiMs help illuminate functional SLiMs in eukaryotic protein families. However, the simplicity of eukaryotic SLiMs makes them appear by chance due to mutational processes not only in eukaryotes but also in pathogenic bacteria and viruses. Further, functional eukaryotic SLiMs are often found in disordered regions. Although proteomes from pathogenic bacteria and viruses have less disorder than eukaryotic proteomes, their proteins can successfully mimic eukaryotic SLiMs and disrupt host cellular function. Identifying important SLiMs in pathogens is difficult but essential for understanding potential host-pathogen interactions. We performed a comparative analysis of structural features for experimentally verified SLiMs from the Eukaryotic Linear Motif (ELM) database across viruses, bacteria, and eukaryotes. Our results revealed that many viral SLiMs and specific motifs found across viruses and eukaryotes, such as some glycosylation motifs, have less disorder. Analyzing the disorder and coil properties of equivalent SLiMs from pathogens and eukaryotes revealed that some motifs are more structured in pathogens than their eukaryotic counterparts and vice versa. These results support a varying mechanism of interaction between pathogens and their eukaryotic hosts for some of the same motifs. Full article
(This article belongs to the Special Issue Computational Biology Applied to Host-Pathogen Interactions)
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Review
Lyme Carditis: From Pathophysiology to Clinical Management
Pathogens 2022, 11(5), 582; https://0-doi-org.brum.beds.ac.uk/10.3390/pathogens11050582 - 15 May 2022
Cited by 1 | Viewed by 566
Abstract
Cardiac involvement is a rare but relevant manifestation of Lyme disease that frequently presents as atrioventricular block (AVB). Immune-mediated injury has been implicated in the pathogenesis of Lyme carditis due to possible cross-reaction between Borrelia burgdorferi antigens and cardiac epitopes. The degree of [...] Read more.
Cardiac involvement is a rare but relevant manifestation of Lyme disease that frequently presents as atrioventricular block (AVB). Immune-mediated injury has been implicated in the pathogenesis of Lyme carditis due to possible cross-reaction between Borrelia burgdorferi antigens and cardiac epitopes. The degree of the AVB can fluctuate rapidly, with two-thirds of patients progressing to complete AVB. Thus, continuous heart rhythm monitoring is essential, and a temporary pacemaker may be necessary. Routinely permanent pacemaker implantation, however, is contraindicated because of the frequent transient nature of the condition. Antibiotic therapy should be initiated as soon as the clinical suspicion of Lyme carditis arises to reduce the duration of the disease and minimize the risk of complications. Diagnosis is challenging and is based on geographical epidemiology, clinical history, signs and symptoms, serological testing, ECG and echocardiographic findings, and exclusion of other pathologies. This paper aims to explain the pathophysiological basis of Lyme carditis, describe its clinical features, and delineate the treatment principles. Full article
(This article belongs to the Special Issue Lyme Borreliosis and tick-borne infections)
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Review
Through the Looking Glass: Genome, Phenome, and Interactome of Salmonella enterica
Pathogens 2022, 11(5), 581; https://0-doi-org.brum.beds.ac.uk/10.3390/pathogens11050581 - 14 May 2022
Viewed by 578
Abstract
This review revisits previous concepts on biological phenomenon contributing to the success of the Salmonella enterica subspecies I as a pathogen and expands upon them to include progress in epidemiology based on whole genome sequencing (WGS). Discussion goes beyond epidemiological uses of WGS [...] Read more.
This review revisits previous concepts on biological phenomenon contributing to the success of the Salmonella enterica subspecies I as a pathogen and expands upon them to include progress in epidemiology based on whole genome sequencing (WGS). Discussion goes beyond epidemiological uses of WGS to consider how phenotype, which is the biological character of an organism, can be correlated with its genotype to develop a knowledge of the interactome. Deciphering genome interactions with proteins, the impact of metabolic flux, epigenetic modifications, and other complex biochemical processes will lead to new therapeutics, control measures, environmental remediations, and improved design of vaccines. Full article
Review
Experimental Hybridization in Leishmania: Tools for the Study of Genetic Exchange
Pathogens 2022, 11(5), 580; https://0-doi-org.brum.beds.ac.uk/10.3390/pathogens11050580 - 14 May 2022
Viewed by 611
Abstract
Despite major advances over the last decade in our understanding of Leishmania reproductive strategies, the sexual cycle in Leishmania has defied direct observation and remains poorly investigated due to experimental constraints. Here, we summarize the findings and conclusions drawn from genetic analysis of [...] Read more.
Despite major advances over the last decade in our understanding of Leishmania reproductive strategies, the sexual cycle in Leishmania has defied direct observation and remains poorly investigated due to experimental constraints. Here, we summarize the findings and conclusions drawn from genetic analysis of experimental hybrids generated in sand flies and highlight the recent advances in generating hybrids in vitro. The ability to hybridize between culture forms of different species and strains of Leishmania should invite more intensive investigation of the mechanisms underlying genetic exchange and provide a rich source of recombinant parasites for future genetic analyses. Full article
(This article belongs to the Special Issue Frontiers in Leishmania)
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