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Extremophilic Microorganisms and Their Communities

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A special issue of Microorganisms (ISSN 2076-2607). This special issue belongs to the section "Environmental Microbiology".

Deadline for manuscript submissions: closed (31 December 2022) | Viewed by 28148

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Dr. Olga V. Golyshina

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Guest Editor

School of Natural Sciences/Centre for Environmental Biotechnology, Bangor University, Deiniol Rd., Bangor LL57 2UW, UK
Interests: microbial diversity; archaea; extremophiles; acidophiles

Dr. Michail M. Yakimov

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Guest Editor

Marine Molecular Microbiology & Biotechnology Institute for Biological Resources and Marine Biotechnologies, CNR-IRBIM Sede di Messina, Spianata San Raineri, 8698122 Messina, Italy
Interests: environmental microbiology; archaea

Special Issue Information

Dear Colleagues,

It is generally appreciated that microorganisms thriving in extreme environments with physical-chemical conditions hostile to common life are taxonomically, genetically, and metabolically diverse and exhibit a plethora of exiting, often counterintuitive, mechanisms of adaptation of a fundamental and applied significance. Environmental parameters where these microorganisms thrive include extreme (high or low) temperatures, pH values, elevated salinities, high hydrostatic pressure, low water activity, high levels of ionizing radiation, and high concentrations of heavy metals or organic solvents. Although extremophilic microbiology is quickly expanding, many aspects still need to be explored and understood, and new microorganisms inhabiting extreme environments still await their isolation and characterization. The aim of this Special Issue is to inform a broader readership on recent studies on extremophilic microorganisms and their communities examined through a range of approaches, from in silico to wet lab investigations and cultivation. As Guest Editors of the Microorganisms Special Issue “Extremophilic Microorganisms and their Communities”, we are looking forward to receiving your valuable contributions in the form of either original research or review papers.

Dr. Olga V. Golyshina
Dr. Michail M. Yakimov
Guest Editors

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Keywords

extremophilic microorganisms
extremophilic bacteria and archaea
extremophilic microbial communities
extreme environments

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Published Papers (9 papers)

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Research

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21 pages, 6458 KiB

Open AccessArticle

Metagenomic Insights into Microbial Community Structure, Function, and Salt Adaptation in Saline Soils of Arid Land, China

by Jianjun Yang, Wenjing Li, Dexiong Teng, Xiaodong Yang, Yijun Zhang and Yan Li

Microorganisms 2022, 10(11), 2183; https://doi.org/10.3390/microorganisms10112183 - 3 Nov 2022

Cited by 18 | Viewed by 3678

Abstract

Soil salinization is spread in the dryland of NW China due to the dry or extreme dry climate. Increased salinization damages the health and function of soil systems and influences the microbial community structure and function. Some studies have been conducted to reveal the microbial community structure and isolate the microorganisms of saline soil or salt-lake sediments in this region. However, the functions of microorganisms and their response to salinization, i.e., their adaptation strategy to a wide salinization range in arid environments, are less understood. Here, we applied metagenomics technology to investigate the microbial community structure, function, and their relationship with salinization, and discussed the adaptative strategy of microorganisms to different saline environments. A total of 42 samples were sequenced on the Illumina PE500 platform. The archaea and bacteria constituted the dominant kingdoms; Actinobacteria, Proteobacteria, Bacteroidetes, and Firmicutes were the dominant bacterial phyla; and Euryarchaeota were the dominant archaeal phylum. The microbial communities showed significant structure divergence according to the salt concentration (saline (mean EC 22 mS/cm) and hypersaline (mean EC 70 mS/cm)), wherein the communities were dominated by bacteria in saline soils and archaea in hypersaline soils. Most of the dominant bacterial representation decreased with salinity, while the archaea increased with salinity. KEGG functional annotation showed that at level 2, the cell motility, environmental adaptation, signal transduction, signaling molecules and interaction, glycan biosynthesis and metabolism, and metabolism of other amino acids were reduced from saline to hypersaline, whereas the metabolism of cofactors and vitamins, folding sorting and degradation, replication and repair, transcription and translation, amino acid biosynthesis, glycolysis/gluconeogenesis, and carbon fixation increased with salinity. The increased salt content decreased the carbohydrate activities of microorganisms. The osmolyte regulation substance synthesis and absorption-related genes were more abundant in saline soils than in hypersaline soils, whereas the Na⁺/H⁺ antiporter genes (mnhB-E) and H⁺/Na⁺-transporting ATPase genes (atpA-F, I, K) were significantly higher in hypersaline soils. This indicated that in saline soils, microorganisms primarily synthesize and/or uptake compatible solutes to cope with osmotic stress, whereas in the hypersaline habitat, the high-salt-in strategy was predicated to be adopted by the halophilic/extremely halophilic microorganisms, coupled with a high abundance of replication and repair, cofactors and vitamin metabolism, nucleotide metabolism, and carbon fixation to provide energy and ensure cell regeneration. In conclusion, increases in salinity influence the microbial communities’ structure and function, as well as the adaptation of microorganisms. Full article

(This article belongs to the Special Issue Extremophilic Microorganisms and Their Communities)

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17 pages, 3802 KiB

Open AccessArticle

Microbial Diversity of a Disused Copper Mine Site (Parys Mountain, UK), Dominated by Intensive Eukaryotic Filamentous Growth

by Marco A. Distaso, Rafael Bargiela, Bethan Johnson, Owen A. McIntosh, Gwion B. Williams, Davey L. Jones, Peter N. Golyshin and Olga V. Golyshina

Microorganisms 2022, 10(9), 1694; https://doi.org/10.3390/microorganisms10091694 - 24 Aug 2022

Cited by 3 | Viewed by 2781

Abstract

The Parys Mountain copper mine (Wales, UK) contains a wide range of discrete environmental microniches with various physicochemical conditions that shape microbial community composition. Our aim was to assess the microbial community in the sediments and overlying water column in an acidic mine drainage (AMD) site containing abundant filamentous biogenic growth via application of a combination of chemical analysis and taxonomic profiling using 16S rRNA gene amplicon sequencing. Our results were then compared to previously studied sites at Parys Mt. Overall, the sediment microbiome showed a dominance of bacteria over archaea, particularly those belonging to Proteobacteria (genera Acidiphilium and Acidisphaera), Acidobacteriota (subgroup 1), Chloroflexota (AD3 cluster), Nitrospirota (Leptospirillum) and the uncultured Planctomycetota/CPIa-3 termite group. Archaea were only present in the sediment in small quantities, being represented by the Terrestrial Miscellaneous Euryarchaeota Group (TMEG), Thermoplasmatales and Ca. Micrarchaeota (Ca. Micracaldota). Bacteria, mostly of the genera Acidiphilium and Leptospirillum, also dominated within the filamentous streamers while archaea were largely absent. This study found pH and dissolved solutes to be the most important parameters correlating with relative proportions of bacteria to archaea in an AMD environment and revealed the abundance patterns of native acidophilic prokaryotes inhabiting Parys Mt sites and their niche specificities. Full article

(This article belongs to the Special Issue Extremophilic Microorganisms and Their Communities)

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18 pages, 3709 KiB

Open AccessArticle

Functional Analysis of Conserved Hypothetical Proteins from the Antarctic Bacterium, Pedobacter cryoconitis Strain BG5 Reveals Protein Cold Adaptation and Thermal Tolerance Strategies

by Makdi Masnoddin, Clemente Michael Wong Vui Ling and Nur Athirah Yusof

Microorganisms 2022, 10(8), 1654; https://doi.org/10.3390/microorganisms10081654 - 16 Aug 2022

Viewed by 2094

Abstract

Pedobacter cryoconitis BG5 is an obligate psychrophilic bacterium that was first isolated on King George Island, Antarctica. Over the last 50 years, the West Antarctic, including King George Island, has been one of the most rapidly warming places on Earth, hence making it an excellent area to measure the resilience of living species in warmed areas exposed to the constantly changing environment due to climate change. This bacterium encodes a genome of approximately 5694 protein-coding genes. However, 35% of the gene models for this species are found to be hypothetical proteins (HP). In this study, three conserved HP genes of P. cryoconitis, designated pcbg5hp1, pcbg5hp2 and pcbg5hp12, were cloned and the proteins were expressed, purified and their functions and structures were evaluated. Real-time quantitative PCR analysis revealed that these genes were expressed constitutively, suggesting a potentially important role where the expression of these genes under an almost constant demand might have some regulatory functions in thermal stress tolerance. Functional analysis showed that these proteins maintained their activities at low and moderate temperatures. Meanwhile, a low citrate synthase aggregation at 43 °C in the presence of PCBG5HP1 suggested the characteristics of chaperone activity. Furthermore, our comparative structural analysis demonstrated that the HPs exhibited cold-adapted traits, most notably increased flexibility in their 3D structures compared to their counterparts. Concurrently, the presence of a disulphide bridge and aromatic clusters was attributed to PCBG5HP1’s unusual protein stability and chaperone activity. Thus, this suggested that the HPs examined in this study acquired strategies to maintain a balance between molecular stability and structural flexibility. Conclusively, this study has established the structure–function relationships of the HPs produced by P. cryoconitis and provided crucial experimental evidence indicating their importance in thermal stress response. Full article

(This article belongs to the Special Issue Extremophilic Microorganisms and Their Communities)

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28 pages, 2866 KiB

Open AccessArticle

Differed Growth Stage Dynamics of Root-Associated Bacterial and Fungal Community Structure Associated with Halophytic Plant Lycium ruthenicum

by Yan Li, Xuemin He, Hongfei Yuan and Guanghui Lv

Microorganisms 2022, 10(8), 1644; https://doi.org/10.3390/microorganisms10081644 - 15 Aug 2022

Cited by 15 | Viewed by 2636

Abstract

Lycium ruthenicum, a halophytic shrub, has been used to remediate saline soils in northwest China. However, little is known about its root-associated microbial community and how it may be affected by the plant’s growth cycle. In this study, we investigate the microbial community structure of L. ruthenicum by examining three root compartments (rhizosphere, rhizoplane, and endosphere) during four growth stages (vegetative, flowering, fruiting, and senescence). The microbial community diversity and composition were determined by Illumina MiSeq sequencing of the 16S V3–V4 and 18S ITS regions. Proteobacteria, Actinobacteria, Bacteroidetes, Planctomycetes, and Acidobacteria were the dominant bacterial phyla, while Ascomycota, Basidiomycota, and Mortierellomycota were the most dominant fungal phyla. The alpha diversity of the bacterial communities was highest in the rhizosphere and decreased from the rhizosphere to the endosphere compartments; the fungal communities did not show a consistent trend. The rhizosphere, rhizoplane, and endosphere had distinct bacterial community structures among the three root compartments and from the bulk soil. Additionally, PERMANOVA indicated that the effect of rhizocompartments explained a large proportion of the total community variation. Differential and biomarker analysis not only revealed that each compartment had unique biomarkers and was enriched for specific bacteria, but also that the biomarkers changed with the plant growth cycle. Fungi were also affected by the rhizocompartment, but to a much less so than bacteria, with significant differences in the community composition along the root compartments observed only during the vegetative and flowering stages. Instead, the growth stages appear to account for most of the fungal community variation as demonstrated by PCoA and NMDS, and supported by differential and biomarker analysis, which revealed that the fungal community composition in the rhizosphere and endosphere were dynamic in response to the growth stage. Many enriched OTUs or biomarkers that were identified in the root compartments were potentially beneficial to the plant, meanwhile, some harmful OTUs were excluded from the root, implying that the host plant can select for beneficial bacteria and fungi, which can promote plant growth or increase salt tolerance. In conclusion, the root compartment and growth stage were both determinant factors in structuring the microbial communities of L. ruthenicum, but the effects were different in bacteria and fungi, suggesting that bacterial and fungal community structures respond differently to these growth factors. Full article

(This article belongs to the Special Issue Extremophilic Microorganisms and Their Communities)

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10 pages, 1519 KiB

Open AccessEditor’s ChoiceArticle

Complex Trophic Interactions in an Acidophilic Microbial Community

by Guntram Weithoff and Elanor M. Bell

Microorganisms 2022, 10(7), 1340; https://doi.org/10.3390/microorganisms10071340 - 2 Jul 2022

Cited by 5 | Viewed by 2465

Abstract

Extreme habitats often harbor specific communities that differ substantially from non-extreme habitats. In many cases, these communities are characterized by archaea, bacteria and protists, whereas the number of species of metazoa and higher plants is relatively low. In extremely acidic habitats, mostly prokaryotes and protists thrive, and only very few metazoa thrive, for example, rotifers. Since many studies have investigated the physiology and ecology of individual species, there is still a gap in research on direct, trophic interactions among extremophiles. To fill this gap, we experimentally studied the trophic interactions between a predatory protist (Actinophrys sol, Heliozoa) and its prey, the rotifers Elosa woralli and Cephalodella sp., the ciliate Urosomoida sp. and the mixotrophic protist Chlamydomonas acidophila (a green phytoflagellate, Chlorophyta). We found substantial predation pressure on all animal prey. High densities of Chlamydomonas acidophila reduced the predation impact on the rotifers by interfering with the feeding behaviour of A. sol. These trophic relations represent a natural case of intraguild predation, with Chlamydomonas acidophila being the common prey and the rotifers/ciliate and A. sol being the intraguild prey and predator, respectively. We further studied this intraguild predation along a resource gradient using Cephalodella sp. as the intraguild prey. The interactions among the three species led to an increase in relative rotifer abundance with increasing resource (Chlamydomonas) densities. By applying a series of laboratory experiments, we revealed the complexity of trophic interactions within a natural extremophilic community. Full article

(This article belongs to the Special Issue Extremophilic Microorganisms and Their Communities)

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21 pages, 1647 KiB

Open AccessArticle

Culturable Bacterial Diversity from the Basaltic Subsurface of the Young Volcanic Island of Surtsey, Iceland

by Pauline Bergsten, Pauline Vannier, Julie Frion, Alan Mougeolle and Viggó Þór Marteinsson

Microorganisms 2022, 10(6), 1177; https://doi.org/10.3390/microorganisms10061177 - 8 Jun 2022

Cited by 5 | Viewed by 3088

Abstract

The oceanic crust is the world’s largest and least explored biosphere on Earth. The basaltic subsurface of Surtsey island in Iceland represents an analog of the warm and newly formed-oceanic crust and offers a great opportunity for discovering novel microorganisms. In this study, we collected borehole fluids, drill cores, and fumarole samples to evaluate the culturable bacterial diversity from the subsurface of the island. Enrichment cultures were performed using different conditions, media and temperatures. A total of 195 bacterial isolates were successfully cultivated, purified, and identified based on MALDI-TOF MS analysis and by 16S rRNA gene sequencing. Six different clades belonging to Firmicutes (40%), Gammaproteobacteria (28.7%), Actinobacteriota (22%), Bacteroidota (4.1%), Alphaproteobacteria (3%), and Deinococcota (2%) were identified. Bacillus (13.3%) was the major genus, followed by Geobacillus (12.33%), Enterobacter (9.23%), Pseudomonas (6.15%), and Halomonas (5.64%). More than 13% of the cultured strains potentially represent novel species based on partial 16S rRNA gene sequences. Phylogenetic analyses revealed that the isolated strains were closely related to species previously detected in soil, seawater, and hydrothermal active sites. The 16S rRNA gene sequences of the strains were aligned against Amplicon Sequence Variants (ASVs) from the previously published 16S rRNA gene amplicon sequence datasets obtained from the same samples. Compared with the culture-independent community composition, only 5 out of 49 phyla were cultivated. However, those five phyla accounted for more than 80% of the ASVs. Only 121 out of a total of 5642 distinct ASVs were culturable (≥98.65% sequence similarity), representing less than 2.15% of the ASVs detected in the amplicon dataset. Here, we support that the subsurface of Surtsey volcano hosts diverse and active microbial communities and that both culture-dependent and -independent methods are essential to improving our insight into such an extreme and complex volcanic environment. Full article

(This article belongs to the Special Issue Extremophilic Microorganisms and Their Communities)

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18 pages, 3843 KiB

Open AccessArticle

Wintertime Simulations Induce Changes in the Structure, Diversity and Function of Antarctic Sea Ice-Associated Microbial Communities

by Violetta La Cono, Francesco Smedile, Francesca Crisafi, Laura Marturano, Stepan V. Toshchakov, Gina La Spada, Ninh Khắc Bản and Michail M. Yakimov

Microorganisms 2022, 10(3), 623; https://doi.org/10.3390/microorganisms10030623 - 15 Mar 2022

Cited by 2 | Viewed by 2719

Abstract

Antarctic sea-ice is exposed to a wide range of environmental conditions during its annual existence; however, there is very little information describing the change in sea-ice-associated microbial communities (SIMCOs) during the changing seasons. It is well known that during the solar seasons, SIMCOs play an important role in the polar carbon-cycle, by increasing the total photosynthetic primary production of the South Ocean and participating in the remineralization of phosphates and nitrogen. What remains poorly understood is the dynamic of SIMCO populations and their ecological contribution to carbon and nutrient cycling throughout the entire annual life of Antarctic sea-ice, especially in winter. Sea ice at this time of the year is an extreme environment, characterized by complete darkness (which stops photosynthesis), extremely low temperatures in its upper horizons (down to −45 °C) and high salinity (up to 150–250 psu) in its brine inclusions, where SIMCOs thrive. Without a permanent station, wintering expeditions in Antarctica are technically difficult; therefore, in this study, the process of autumn freezing was modelled under laboratory conditions, and the resulting ‘young ice’ was further incubated in cold and darkness for one month. The ice formation experiment was primarily designed to reproduce two critical conditions: (i) total darkness, causing the photosynthesis to cease, and (ii) the presence of a large amount of algae-derived organic matter. As expected, in the absence of photosynthesis, the activity of aerobic heterotrophs quickly created micro-oxic conditions, which caused the emergence of new players, namely facultative anaerobic and anaerobic microorganisms. Following this finding, we can state that Antarctic pack-ice and its surrounding ambient (under-ice seawater and platelet ice) are likely to be very dynamic and can quickly respond to environmental changes caused by the seasonal fluctuations. Given the size of Antarctic pack-ice, even in complete darkness and cessation of photosynthesis, its ecosystem appears to remain active, continuing to participate in global carbon-and-sulfur cycling under harsh conditions. Full article

(This article belongs to the Special Issue Extremophilic Microorganisms and Their Communities)

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20 pages, 1443 KiB

Open AccessArticle

The Effects of Freeze-Thaw and UVC Radiation on Microbial Survivability in a Selected Mars-like Environment

by Daniel Keaney, Brigid Lucey, Noreen Quinn and Karen Finn

Microorganisms 2022, 10(3), 576; https://doi.org/10.3390/microorganisms10030576 - 7 Mar 2022

Cited by 4 | Viewed by 3750

Abstract

The purpose of this study was to determine survivability of Escherichia coli, Deinococcus radiodurans and Paraburkholderia fungorum under Mars-simulated conditions for freeze-thawing (−80 °C to +30 °C) and UV exposure alone and in combination. E. coli ATCC 25922, D. radiodurans and P. fungorum remained viable following 20 successive freeze-thaw cycles, exhibiting viabilities of 2.3%, 96% and 72.6%, respectively. E. coli ATCC 9079 was non-recoverable by cycle 9. When exposed to UV irradiation, cells withstood doses of 870 J/m² (E. coli ATCC 25922), 200 J/m² (E. coli ATCC 9079), 50,760 J/m² (D. radiodurans) and 44,415 J/m² (P. fungorum). Data suggests P. fungorum is highly UV-resistant. Combined freeze-thawing with UV irradiation showed freezing increased UV resistance in E. coli ATCC 25922, E. coli DSM 9079 and D. radiodurans by 6-fold, 30-fold and 1.2-fold, respectively. Conversely, freezing caused P. fungorum to exhibit a 1.75-fold increase in UV susceptibility. Strain-dependent experimentation demonstrated that freezing increases UV resistance and prolongs survival. These findings suggest that exposure to short wavelength UV rays (254 nm) and temperature cycles resembling the daily fluctuating conditions on Mars do not significantly affect survival of D. radiodurans, P. fungorum and E. coli ATCC 25922 following 20 days of exposure. Full article

(This article belongs to the Special Issue Extremophilic Microorganisms and Their Communities)

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24 pages, 2404 KiB

Open AccessReview

Glacial Water: A Dynamic Microbial Medium

by Gilda Varliero, Pedro H. Lebre, Beat Frey, Andrew G. Fountain, Alexandre M. Anesio and Don A. Cowan

Microorganisms 2023, 11(5), 1153; https://doi.org/10.3390/microorganisms11051153 - 28 Apr 2023

Cited by 6 | Viewed by 3362

Abstract

Microbial communities and nutrient dynamics in glaciers and ice sheets continuously change as the hydrological conditions within and on the ice change. Glaciers and ice sheets can be considered bioreactors as microbiomes transform nutrients that enter these icy systems and alter the meltwater chemistry. Global warming is increasing meltwater discharge, affecting nutrient and cell export, and altering proglacial systems. In this review, we integrate the current understanding of glacial hydrology, microbial activity, and nutrient and carbon dynamics to highlight their interdependence and variability on daily and seasonal time scales, as well as their impact on proglacial environments. Full article

(This article belongs to the Special Issue Extremophilic Microorganisms and Their Communities)

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