Genetics and Genomics of Acidophiles

A special issue of Genes (ISSN 2073-4425). This special issue belongs to the section "Microbial Genetics and Genomics".

Deadline for manuscript submissions: closed (3 July 2020) | Viewed by 23123

Special Issue Editors


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Guest Editor
Department of Microbiology and Immunology, Montana State University, Bozeman, MT 59717, USA
Interests: hyperthermophiles; acidophiles; extremophiles; elemental sulfur reduction; hydrogen metabolism; origin of life; metalloenzyme evolution; geobiology

E-Mail Website
Guest Editor
Department of Microbiology and Immunology, Montana State University, Bozeman, MT 59717, USA
Interests: Archaea; thermophiles; acidophiles; ecological distributions; community assembly; subsurface environments; thermal springs; evolutionary ecology; geobiological interactions

E-Mail Website
Guest Editor
Department of Microbiology and Immunology, Montana State University, Bozeman, MT 59717, USA
Interests: extremophiles; thermophiles; acidophiles; sulfur metabolism; iron metabolism; bioenergetics; physiology; subsurface biosphere

Special Issue Information

Dear Colleagues,

Acidic environments and the organisms that they host are of significant interest to disciplines ranging from microbiology, biotechnology, Earth sciences, to astrobiology, and have been subject to extensive research to understand the processes that contribute to their formation and the adaptations that allow for their habitation. Acidophiles, organisms that grow optimally at acidic pH, are distributed across all three domains of life and exhibit substantial physiological diversity. Acidophiles grow in environments with pH as low as 0 and at temperatures as high as ~90 oC. As such, they display a wide diversity of metabolic lifestyles and physiological adaptations. Further, the metabolic activities of lithotrophic acidophiles are important in the formation of acidic environments where they influence metal cycling and metal availability. The insights gained from the study of acidophiles have provided new insights into the physiological limits of life and have uncovered unique adaptations that allow life to thrive under pH extremes.  

The low taxonomic diversity of communities in acidic habitats has allowed for the development and application of cutting edge technologies in environmental microbiology such as metagenomics, metatranscriptomics, and proteomics. Moreover, the low diversity of acidophilic communities has allowed for testing of macrobiological theories on microbial ecosystems, including the concept of island biogeography. These advances have led to numerous new insights into the physiological diversity of acidophiles and the ecological drivers of their diversification. However, numerous key questions regarding acidophiles remain unanswered including: When did acidophiles and their habitats evolve? What role has horizontal gene transfer had in promoting acidophily? What regulatory systems underpin the ability of acidophiles to survive and persist in acidic environments? How do acidophile protein systems facilitate microbe-mineral interactions and influence biogeochemical cycles? What is the relationship between acidophilic adaptation and aerobic metabolism? What is the most acidic habitat tolerated by an anaerobe? How have viruses evolved alongside their acidophilic hosts?

This Special Issue is focused on the genetics and genomics of acidophiles and their viruses and seeks studies that focus on comparative genomics, genetic systems, the genetic/genomic mechanisms of acidophilic adaptations and/or microbe-mineral interactions, genomic evolution, and genetic exchange, among other interrelated topics. Submissions of original research studies and reviews related to the above, or related, topics and questions regarding acidophiles are invited to be featured as part of this Special Issue in Genes.

Prof. Eric Boyd
Dr. Dan Colman
Dr. Maximiliano Amenabar
Guest Editors

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Keywords

  • Acidophiles
  • Archaea
  • Bacteria
  • Eukaryotes
  • viruses
  • geochemical cycles
  • metals
  • ore leaching
  • aerobes

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Published Papers (6 papers)

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Research

24 pages, 4648 KiB  
Article
From Laboratory towards Industrial Operation: Biomarkers for Acidophilic Metabolic Activity in Bioleaching Systems
by Sabrina Marín, Mayra Cortés, Mauricio Acosta, Karla Delgado, Camila Escuti, Diego Ayma and Cecilia Demergasso
Genes 2021, 12(4), 474; https://doi.org/10.3390/genes12040474 - 25 Mar 2021
Cited by 8 | Viewed by 2434
Abstract
In the actual mining scenario, copper bioleaching, mainly raw mined material known as run-of-mine (ROM) copper bioleaching, is the best alternative for the treatment of marginal resources that are not currently considered part of the profitable reserves because of the cost associated with [...] Read more.
In the actual mining scenario, copper bioleaching, mainly raw mined material known as run-of-mine (ROM) copper bioleaching, is the best alternative for the treatment of marginal resources that are not currently considered part of the profitable reserves because of the cost associated with leading technologies in copper extraction. It is foreseen that bioleaching will play a complementary role in either concentration—as it does in Minera Escondida Ltd. (MEL)—or chloride main leaching plants. In that way, it will be possible to maximize mines with installed solvent-extraction and electrowinning capacities that have not been operative since the depletion of their oxide ores. One of the main obstacles for widening bioleaching technology applications is the lack of knowledge about the key events and the attributes of the technology’s critical events at the industrial level and mainly in ROM copper bioleaching industrial operations. It is relevant to assess the bed environment where the bacteria–mineral interaction occurs to learn about the limiting factors determining the leaching rate. Thus, due to inability to accurately determine in-situ key variables, their indirect assessment was evaluated by quantifying microbial metabolic-associated responses. Several candidate marker genes were selected to represent the predominant components of the microbial community inhabiting the industrial heap and the metabolisms involved in microbial responses to changes in the heap environment that affect the process performance. The microbial community’s predominant components were Acidithiobacillus ferrooxidans, At. thiooxidans, Leptospirillum ferriphilum, and Sulfobacillus sp. Oxygen reduction, CO2 and N2 fixation/uptake, iron and sulfur oxidation, and response to osmotic stress were the metabolisms selected regarding research results previously reported in the system. After that, qPCR primers for each candidate gene were designed and validated. The expression profile of the selected genes vs. environmental key variables in pure cultures, column-leaching tests, and the industrial bioleaching heap was defined. We presented the results obtained from the industrial validation of the marker genes selected for assessing CO2 and N2 availability, osmotic stress response, as well as ferrous iron and sulfur oxidation activity in the bioleaching heap process of MEL. We demonstrated that molecular markers are useful for assessing limiting factors like nutrients and air supply, and the impact of the quality of recycled solutions. We also learned about the attributes of variables like CO2, ammonium, and sulfate levels that affect the industrial ROM-scale operation. Full article
(This article belongs to the Special Issue Genetics and Genomics of Acidophiles)
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18 pages, 1961 KiB  
Article
Unlocking Survival Mechanisms for Metal and Oxidative Stress in the Extremely Acidophilic, Halotolerant Acidihalobacter Genus
by Himel Nahreen Khaleque, Homayoun Fathollazadeh, Carolina González, Raihan Shafique, Anna H. Kaksonen, David S. Holmes and Elizabeth L.J. Watkin
Genes 2020, 11(12), 1392; https://doi.org/10.3390/genes11121392 - 24 Nov 2020
Cited by 10 | Viewed by 3360
Abstract
Microorganisms used for the biohydrometallurgical extraction of metals from minerals must be able to survive high levels of metal and oxidative stress found in bioleaching environments. The Acidihalobacter genus consists of four species of halotolerant, iron–sulfur-oxidizing acidophiles that are unique in their ability [...] Read more.
Microorganisms used for the biohydrometallurgical extraction of metals from minerals must be able to survive high levels of metal and oxidative stress found in bioleaching environments. The Acidihalobacter genus consists of four species of halotolerant, iron–sulfur-oxidizing acidophiles that are unique in their ability to tolerate chloride and acid stress while simultaneously bioleaching minerals. This paper uses bioinformatic tools to predict the genes and mechanisms used by Acidihalobacter members in their defense against a wide range of metals and oxidative stress. Analysis revealed the presence of multiple conserved mechanisms of metal tolerance. Ac. yilgarnensis F5T, the only member of this genus that oxidizes the mineral chalcopyrite, contained a 39.9 Kb gene cluster consisting of 40 genes encoding mobile elements and an array of proteins with direct functions in copper resistance. The analysis also revealed multiple strategies that the Acidihalobacter members can use to tolerate high levels of oxidative stress. Three of the Acidihalobacter genomes were found to contain genes encoding catalases, which are not common to acidophilic microorganisms. Of particular interest was a rubrerythrin genomic cluster containing genes that have a polyphyletic origin of stress-related functions. Full article
(This article belongs to the Special Issue Genetics and Genomics of Acidophiles)
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30 pages, 3500 KiB  
Article
Genome Mining of the Genus Streptacidiphilus for Biosynthetic and Biodegradation Potential
by Adeel Malik, Yu Ri Kim and Seung Bum Kim
Genes 2020, 11(10), 1166; https://doi.org/10.3390/genes11101166 - 3 Oct 2020
Cited by 15 | Viewed by 3531
Abstract
The genus Streptacidiphilus represents a group of acidophilic actinobacteria within the family Streptomycetaceae, and currently encompasses 15 validly named species, which include five recent additions within the last two years. Considering the potential of the related genera within the family, namely Streptomyces [...] Read more.
The genus Streptacidiphilus represents a group of acidophilic actinobacteria within the family Streptomycetaceae, and currently encompasses 15 validly named species, which include five recent additions within the last two years. Considering the potential of the related genera within the family, namely Streptomyces and Kitasatospora, these relatively new members of the family can also be a promising source for novel secondary metabolites. At present, 15 genome data for 11 species from this genus are available, which can provide valuable information on their biology including the potential for metabolite production as well as enzymatic activities in comparison to the neighboring taxa. In this study, the genome sequences of 11 Streptacidiphilus species were subjected to the comparative analysis together with selected Streptomyces and Kitasatospora genomes. This study represents the first comprehensive comparative genomic analysis of the genus Streptacidiphilus. The results indicate that the genomes of Streptacidiphilus contained various secondary metabolite (SM) producing biosynthetic gene clusters (BGCs), some of them exclusively identified in Streptacidiphilus only. Several of these clusters may potentially code for SMs that may have a broad range of bioactivities, such as antibacterial, antifungal, antimalarial and antitumor activities. The biodegradation capabilities of Streptacidiphilus were also explored by investigating the hydrolytic enzymes for complex carbohydrates. Although all genomes were enriched with carbohydrate-active enzymes (CAZymes), their numbers in the genomes of some strains such as Streptacidiphilus carbonis NBRC 100919T were higher as compared to well-known carbohydrate degrading organisms. These distinctive features of each Streptacidiphilus species make them interesting candidates for future studies with respect to their potential for SM production and enzymatic activities. Full article
(This article belongs to the Special Issue Genetics and Genomics of Acidophiles)
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19 pages, 4085 KiB  
Article
Determinants of Copper Resistance in Acidithiobacillus Ferrivorans ACH Isolated from the Chilean Altiplano
by Sergio Barahona, Juan Castro-Severyn, Cristina Dorador, Claudia Saavedra and Francisco Remonsellez
Genes 2020, 11(8), 844; https://doi.org/10.3390/genes11080844 - 24 Jul 2020
Cited by 12 | Viewed by 3231
Abstract
The use of microorganisms in mining processes is a technology widely employed around the world. Leaching bacteria are characterized by having resistance mechanisms for several metals found in their acidic environments, some of which have been partially described in the Acidithiobacillus genus (mainly [...] Read more.
The use of microorganisms in mining processes is a technology widely employed around the world. Leaching bacteria are characterized by having resistance mechanisms for several metals found in their acidic environments, some of which have been partially described in the Acidithiobacillus genus (mainly on ferrooxidans species). However, the response to copper has not been studied in the psychrotolerant Acidithiobacillus ferrivorans strains. Therefore, we propose to elucidate the response mechanisms of A. ferrivorans ACH to high copper concentrations (0–800 mM), describing its genetic repertoire and transcriptional regulation. Our results show that A. ferrivorans ACH can grow in up to 400 mM of copper. Moreover, we found the presence of several copper-related makers, belonging to cop and cus systems, as well as rusticyanins and periplasmatic acop protein in the genome. Interestingly, the ACH strain is the only one in which we find three copies of copB and copZ genes. Moreover, transcriptional expression showed an up-regulation response (acop, copZ, cusA, rusA, and rusB) to high copper concentrations. Finally, our results support the important role of these genes in A. ferrivorans copper stress resistance, promoting the use of the ACH strain in industrial leaching under low temperatures, which could decrease the activation times of oxidation processes and the energy costs. Full article
(This article belongs to the Special Issue Genetics and Genomics of Acidophiles)
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23 pages, 3814 KiB  
Article
Evolution of Predicted Acid Resistance Mechanisms in the Extremely Acidophilic Leptospirillum Genus
by Eva Vergara, Gonzalo Neira, Carolina González, Diego Cortez, Mark Dopson and David S. Holmes
Genes 2020, 11(4), 389; https://doi.org/10.3390/genes11040389 - 3 Apr 2020
Cited by 26 | Viewed by 4680
Abstract
Organisms that thrive in extremely acidic environments (≤pH 3.5) are of widespread importance in industrial applications, environmental issues, and evolutionary studies. Leptospirillum spp. constitute the only extremely acidophilic microbes in the phylogenetically deep-rooted bacterial phylum Nitrospirae. Leptospirilli are Gram-negative, obligatory chemolithoautotrophic, aerobic, ferrous [...] Read more.
Organisms that thrive in extremely acidic environments (≤pH 3.5) are of widespread importance in industrial applications, environmental issues, and evolutionary studies. Leptospirillum spp. constitute the only extremely acidophilic microbes in the phylogenetically deep-rooted bacterial phylum Nitrospirae. Leptospirilli are Gram-negative, obligatory chemolithoautotrophic, aerobic, ferrous iron oxidizers. This paper predicts genes that Leptospirilli use to survive at low pH and infers their evolutionary trajectory. Phylogenetic and other bioinformatic approaches suggest that these genes can be classified into (i) “first line of defense”, involved in the prevention of the entry of protons into the cell, and (ii) neutralization or expulsion of protons that enter the cell. The first line of defense includes potassium transporters, predicted to form an inside positive membrane potential, spermidines, hopanoids, and Slps (starvation-inducible outer membrane proteins). The “second line of defense“ includes proton pumps and enzymes that consume protons. Maximum parsimony, clustering methods, and gene alignments are used to infer the evolutionary trajectory that potentially enabled the ancestral Leptospirillum to transition from a postulated circum-neutral pH environment to an extremely acidic one. The hypothesized trajectory includes gene gains/loss events driven extensively by horizontal gene transfer, gene duplications, gene mutations, and genomic rearrangements. Full article
(This article belongs to the Special Issue Genetics and Genomics of Acidophiles)
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11 pages, 2821 KiB  
Article
Diversity of “Ca. Micrarchaeota” in Two Distinct Types of Acidic Environments and Their Associations with Thermoplasmatales
by Olga V. Golyshina, Rafael Bargiela, Stepan V. Toshchakov, Nikolay A. Chernyh, Soshila Ramayah, Aleksei A. Korzhenkov, Ilya V. Kublanov and Peter N. Golyshin
Genes 2019, 10(6), 461; https://doi.org/10.3390/genes10060461 - 15 Jun 2019
Cited by 19 | Viewed by 4402
Abstract
Candidatus Micrarchaeota” are widely distributed in acidic environments; however, their cultivability and our understanding of their interactions with potential hosts are very limited. Their habitats were so far attributed with acidic sites, soils, peats, freshwater systems, and hypersaline mats. Using cultivation and [...] Read more.
Candidatus Micrarchaeota” are widely distributed in acidic environments; however, their cultivability and our understanding of their interactions with potential hosts are very limited. Their habitats were so far attributed with acidic sites, soils, peats, freshwater systems, and hypersaline mats. Using cultivation and culture-independent approaches (16S rRNA gene clonal libraries, high-throughput amplicon sequencing of V3-V4 region of 16S rRNA genes), we surveyed the occurrence of these archaea in geothermal areas on Kamchatka Peninsula and Kunashir Island and assessed their taxonomic diversity in relation with another type of low-pH environment, acid mine drainage stream (Wales, UK). We detected “Ca. Micrarchaeota” in thermophilic heterotrophic enrichment cultures of Kunashir and Kamchatka that appeared as two different phylotypes, namely “Ca. Mancarchaeum acidiphilum”-, and ARMAN-2-related, alongside their potential hosts, Cuniculiplasma spp. and other Thermoplasmatales archaea without defined taxonomic position. These clusters of “Ca. Micrarchaeota” together with three other groups were also present in mesophilic acid mine drainage community. Present work expands our knowledge on the diversity of “Ca. Micrarchaeota” in thermophilic and mesophilic acidic environments, suggests cultivability patterns of acidophilic archaea and establishes potential links between low-abundance species of thermophilic “Ca. Micrarchaeota” and certain Thermoplasmatales, such as Cuniculiplasma spp. in situ. Full article
(This article belongs to the Special Issue Genetics and Genomics of Acidophiles)
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