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"Barton, Hazel"
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Antibiotic Resistance Is Prevalent in an Isolated Cave Microbiome
Antibiotic resistance is a global challenge that impacts all pharmaceutically used antibiotics. The origin of the genes associated with this resistance is of significant importance to our understanding of the evolution and dissemination of antibiotic resistance in pathogens. A growing body of evidence implicates environmental organisms as reservoirs of these resistance genes; however, the role of anthropogenic use of antibiotics in the emergence of these genes is controversial. We report a screen of a sample of the culturable microbiome of Lechuguilla Cave, New Mexico, in a region of the cave that has been isolated for over 4 million years. We report that, like surface microbes, these bacteria were highly resistant to antibiotics; some strains were resistant to 14 different commercially available antibiotics. Resistance was detected to a wide range of structurally different antibiotics including daptomycin, an antibiotic of last resort in the treatment of drug resistant Gram-positive pathogens. Enzyme-mediated mechanisms of resistance were also discovered for natural and semi-synthetic macrolide antibiotics via glycosylation and through a kinase-mediated phosphorylation mechanism. Sequencing of the genome of one of the resistant bacteria identified a macrolide kinase encoding gene and characterization of its product revealed it to be related to a known family of kinases circulating in modern drug resistant pathogens. The implications of this study are significant to our understanding of the prevalence of resistance, even in microbiomes isolated from human use of antibiotics. This supports a growing understanding that antibiotic resistance is natural, ancient, and hard wired in the microbial pangenome.
Journal Article
A diverse intrinsic antibiotic resistome from a cave bacterium
Antibiotic resistance is ancient and widespread in environmental bacteria. These are therefore reservoirs of resistance elements and reflective of the natural history of antibiotics and resistance. In a previous study, we discovered that multi-drug resistance is common in bacteria isolated from Lechuguilla Cave, an underground ecosystem that has been isolated from the surface for over 4 Myr. Here we use whole-genome sequencing, functional genomics and biochemical assays to reveal the intrinsic resistome of
Paenibacillus
sp. LC231, a cave bacterial isolate that is resistant to most clinically used antibiotics. We systematically link resistance phenotype to genotype and in doing so, identify 18 chromosomal resistance elements, including five determinants without characterized homologues and three mechanisms not previously shown to be involved in antibiotic resistance. A resistome comparison across related surface
Paenibacillus
affirms the conservation of resistance over millions of years and establishes the longevity of these genes in this genus.
Antibiotic resistance is common in environmental bacteria, including those living in isolated caves. Here, Pawlowski
et al
. study one of these bacterial strains, showing that it is resistant to most clinically used antibiotics through a remarkable variety of mechanisms, some of which are new to science.
Journal Article
The diversity of cellular systems involved in carbonate precipitation by Escherichia coli
Climate change is increasing the need to limit levels of anthropogenic CO 2 released into the atmosphere. One approach being investigated is to generate products based on microbially induced carbonate precipitation (MICP), which can trap CO 2 as CaCO 3 . We recently identified a novel MICP pathway in bacteria that is initiated by Ca 2+ toxicity in cells, causing extracellular CO 2 to be trapped as CO 3 2- by Escherichia coli, although the yield of precipitated CaCO 3 remained low (in the milligram range). In this work, we used the E. coli Keio gene knock-out library to identify 54 genes involved in MICP in E. coli, which could be broadly characterized into four groups: central metabolism, iron metabolism, cell architecture, and transport. The role of central metabolism appears to be crucial in maintaining alkaline conditions surrounding the cell that promote CaCO 3 precipitation. The role of iron metabolism was less clear, although the results suggest that growth rate influences the initiation of MICP. While the impact of repeating polymeric structures on cell surfaces promoting MICP is well established, our results suggest that other structural features may play a role, including fimbriae and flagella. Finally, the results confirmed that Ca 2+ transport is central to MICP under calcium stress. The results further suggest that the ZntB efflux pump may play a previously unidentified role in Ca 2+ transport in E. coli. By overexpressing some of these genes, our work suggests that there are several previously unidentified cellular mechanisms that could serve as a target for enhanced MICP in E. coli. By incorporating these processes into MICP pathways in E. coli, it may be possible to increase the volume of CO 2 fixed using this pathway and yield potentially new products that can replace CO 2 intensive products, such as precipitated calcium carbonates (PCCs) for industry.
Journal Article
Comparison of the White-Nose Syndrome Agent Pseudogymnoascus destructans to Cave-Dwelling Relatives Suggests Reduced Saprotrophic Enzyme Activity
White-nose Syndrome (WNS) is an emerging infectious mycosis that has impacted multiple species of North American bats since its initial discovery in 2006, yet the physiology of the causal agent, the psychrophilic fungus Pseudogymnoascus destructans ( = Geomyces destructans), is not well understood. We investigated the ability of P. destructans to secrete enzymes that could permit environmental growth or affect pathogenesis and compared enzyme activity across several Pseudogymnoascus species isolated from both hibernating bats and cave sediments. We found that P. destructans produced enzymes that could be beneficial in either a pathogenic or saprotrophic context, such as lipases, hemolysins, and urease, as well as chitinase and cellulases, which could aid in saprotrophic growth. The WNS pathogen showed significantly lower activity for urease and endoglucanase compared to con-generic species (Pseudogymnoascus), which may indicate a shift in selective pressure to the detriment of P. destructans' saprotrophic ability. Based on the positive function of multiple saprotrophic enzymes, the causal agent of White-nose Syndrome shows potential for environmental growth on a variety of substrates found in caves, albeit at a reduced level compared to environmental strains. Our data suggest that if P. destructans emerged as an opportunistic infection from an environmental source, co-evolution with its host may have led to a reduced capacity for saprotrophic growth.
Journal Article
Safe and effective disinfection of show cave infrastructure in a time of COVID-19
The COVID-19 pandemic, caused by the novel coronavirus SARS-CoV-2, has been responsible for over 650,000 deaths worldwide. Transmission of SARS-CoV-2 occurs primarily through airborne transmission or direct human contact, demonstrating the importance of social distancing measures and the use of face masks to prevent infection. Nonetheless, the persistence of coronavirus on surfaces means that disinfection is important to limit the possibility of contact transmission. In this paper, the potential for various surfaces in show caves to serve as sources for SARS-CoV-2 infection is examined. Given the isoelectric potential (pI) of SARS and SARS-like coronaviruses, it is likely that they are adsorbed via electrochemical interactions to (limestone) rock surfaces, where the high humidity, pH and presence of biocarbonate ions will quickly lead to inactivation. Nonetheless, show caves contain infrastructure made of other non-porous surfaces that are more permissive for maintaining coronavirus viability. The 423 antiviral products approved by the US Environmental Protection Agency (EPA) were curated into 23 antiviral chemistries, which were further classified based on their potential to be hazardous, impact cave features or ecosystems, and those compounds likely to have the minimum impact on caves. The results suggest that alcohols (70% ethanol), organic acids (citric and lactic acid) and dilute hypochlorite represent the best disinfectants for in-cave use on non-porous surfaces. These disinfectants are able to inactivate coronaviruses inecosystems.
Journal Article
Women Are Underrepresented and Receive Differential Outcomes at ASM Journals: a Six-Year Retrospective Analysis
Barriers in science and academia have prevented women from becoming researchers and experts that are viewed as equivalent to their colleagues who are men. We evaluated the participation and success of women researchers at ASM journals to better understand their success in the field of microbiology. We found that women are underrepresented as expert scientists at ASM journals. This is, in part, due to a combination of both low submissions from senior women authors and more negative outcomes on submitted manuscripts for women compared to men. Despite 50% of biology Ph.D. graduates being women, the number of women that advance in academia decreases at each level (e.g., from graduate to postdoctorate to tenure track). Recently, scientific societies and publishers have begun examining internal submissions data to evaluate representation and evaluation of women in their peer review processes; however, representation and attitudes differ by scientific field, and to date, no studies have investigated academic publishing in the field of microbiology. Using manuscripts submitted between January 2012 and August 2018 to the 15 journals published by the American Society for Microbiology (ASM), we describe the representation of women at ASM journals and the outcomes of their manuscripts. Senior women authors at ASM journals were underrepresented compared to global and society estimates of microbiology researchers. Additionally, manuscripts submitted by corresponding authors that were women received more negative outcomes than those submitted by men. These negative outcomes were somewhat mediated by whether or not the corresponding author was based in the United States and by the type of institution for United States-based authors. Nonetheless, the pattern for women corresponding authors to receive more negative outcomes on their submitted manuscripts held. We conclude with suggestions to improve the representation of women and decrease structural penalties against women. IMPORTANCE Barriers in science and academia have prevented women from becoming researchers and experts that are viewed as equivalent to their colleagues who are men. We evaluated the participation and success of women researchers at ASM journals to better understand their success in the field of microbiology. We found that women are underrepresented as expert scientists at ASM journals. This is, in part, due to a combination of both low submissions from senior women authors and more negative outcomes on submitted manuscripts for women compared to men.
Journal Article
Enhanced terrestrial Fe(II) mobilization identified through a novel mechanism of microbially driven cave formation in Fe(III)-rich rocks
Most cave formation requires mass separation from a host rock in a process that operates outward from permeable pathways to create the cave void. Given the poor solubility of Fe(III) phases, such processes are insufficient to account for the significant iron formation caves (IFCs) seen in Brazilian banded iron formations (BIF) and associated rock. In this study we demonstrate that microbially-mediated reductive Fe(III) dissolution is solubilizing the poorly soluble Fe(III) phases to soluble Fe(II) in the anoxic zone behind cave walls. The resultant Fe(III)-depleted material (termed
sub muros
) is unable to maintain the structural integrity of the walls and repeated rounds of wall collapse lead to formation of the cave void in an active, measurable process. This mechanism may move significant quantities of Fe(II) into ground water and may help to explain the mechanism of BIF dissolution and REE enrichment in the generation of canga. The role of Fe(III) reducing microorganism and mass separation behind the walls (outward-in, rather than inward-out) is not only a novel mechanism of speleogenesis, but it also may identify a previously overlooked source of continental Fe that may have contributed to Archaean BIF formation.
Journal Article
The impact of sample processing and media chemistry on the culturable diversity of bacteria isolated from a cave
Although molecular approaches can identify members of microbial communities in the environment, genomic information does not necessarily correlate with environmental phenotype. Understanding functional roles can be done by cultivating representative species, yet the culturablility of bacteria from caves remains low, at 0.02%, limiting our understanding of microbial community interactions and processes. We have investigated several factors influencing culturability of bacteria from a single sample location in Maxwelton Sink Cave, WV, USA. Extended incubation of inoculated plates showed a significant increase in colony counts from two to four weeks, indicating that extended incubations increase culturability. There were no significant differences in plate counts or diversity measures when the sample was suspended in different buffers prior to cultivation, while samples plated immediately after collection demonstrated higher culturability. Although supplementing the media with antibiotics reduced colony counts and cultured diversity, these plates did appear to contain a higher proportion of slow-growing oligotrophs. Finally, among a selection of culture media used, pyruvate agar showed the highest culturability and bacterial diversity, which may be a result of the oxygen radical scavenging effects of pyruvate. By identifying methods that improve culturable diversity, we hope to further understand the roles played by bacteria in cave communities, and test hypotheses that are best assessed using culture-based methods, such as screening for bioactive compounds or confirming in situ metabolic strategies.
Journal Article
Exceptional variety of baryte-celestine-series speleothems in Lechuguilla Cave (New Mexico, USA)
An inventory of speleothems primarily composed of the closely related sulfate minerals baryte (BaSO4) and celestine (SrSO4) in Lechuguilla Cave (New Mexico, USA) has revealed an extraordinary variety. This includes subaerial stalactites, stalagmites, flowstone, coralloids, wall crusts, floor crystals, snow, frostwork, and subaqueous pool crystals. Large baryte and celestine crystals have also been documented in hydrothermal veins in the host rock, predating the cave and truncated when intersected by it. The respective carbonate mineral phases witherite (BaCO3) and strontianite (SrCO3), in contrast, were found to be rare in the studied speleothem samples, representing the first confirmed records from this cave. Baryte speleothems are typically composed of pure baryte, whereas celestine is usually syntactically intergrown with small baryte crystals and forms part of the most diverse assemblages of secondary cave minerals recorded in the cave to date, including species of the following mineral groups: carbonates (calcite, dolomite, aragonite, huntite, hydromagnesite, strontianite, and witherite), sulfates (gypsum), oxides and hydroxides (undetermined Mn/Fe-oxides or hydroxides), silicates (quartz, chalcedony, opal/cristobalite/tridymite, and montmorillonite), halogenides (fluorite), and vanadates (metatyuyamunite). Based on 230Th/U-series dating of directly associated carbonate minerals and gypsum, the age of formation of the various types of baryte and celestine speleothems was constrained to a range from the Middle Pleistocene to the Holocene. This confirms a formation during the ongoing post-hydrothermal and post-SAS (sulphuric acid speleogenesis) phase of epigenic normal temperature cave development. Six samples fall outside the dating range with close to secular equilibrium isotope ratios and are thus likely older than ~600 ka. While baryte stalactites, stalagmites, flowstone, and pool crystals are still forming, celestine minerogenesis, except for some of the coralloids, appears to have largely ceased in Lechuguilla Cave.
Journal Article