Leave no stone unturned: individually adapted xerotolerant Thaumarchaeota sheltered below the boulders of the Atacama Desert hyperarid core

Abstract Background The hyperarid core of the Atacama Desert is an extremely harsh environment thought to be colonized by only a few heterotrophic bacterial species. Current concepts for understanding this extreme ecosystem are mainly based on the diversity of these few species, yet a substantial area of the Atacama Desert hyperarid topsoil is covered by expansive boulder accumulations, whose underlying microbiomes have not been investigated so far. With the hypothesis that these sheltered soils harbor uniquely adapted microbiomes, we compared metagenomes and geochemistry between soils below and beside boulders across three distantly located boulder accumulations in the Atacama Desert hyperarid core. Results Genome-resolved metagenomics of eleven samples revealed substantially different microbial communities in soils below and beside boulders, despite the presence of shared species. Archaea were found in significantly higher relative abundance below the boulders across all samples within distances of up to 205 km. These key taxa belong to a novel genus of ammonia-oxidizing Thaumarchaeota, Candidatus Nitrosodeserticola. We resolved eight mid-to-high quality genomes of this genus and used comparative genomics to analyze its pangenome and site-specific adaptations. Ca. Nitrosodeserticola genomes contain genes for ammonia oxidation, the 3-hydroxypropionate/4-hydroxybutyrate carbon fixation pathway, and acetate utilization indicating a chemolithoautotrophic and mixotrophic lifestyle. They also possess the capacity for tolerating extreme environmental conditions as highlighted by the presence of genes against oxidative stress and DNA damage. Site-specific adaptations of the genomes included the presence of additional genes for heavy metal transporters, multiple types of ATP synthases, and divergent genes for aquaporins. Conclusion We provide the first genomic characterization of hyperarid soil microbiomes below the boulders in the Atacama Desert, and report abundant and highly adapted Thaumarchaeaota with ammonia oxidation and carbon fixation potential. Ca. Nitrosodeserticola genomes provide the first metabolic and physiological insight into a thaumarchaeal lineage found in globally distributed terrestrial habitats characterized by various environmental stresses. We consequently expand not only the known genetic repertoire of Thaumarchaeota but also the diversity and microbiome functioning in hyperarid ecosystems.

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Leave no stone unturned: The hidden potential of carbon and nitrogen cycling by novel, highly adapted Thaumarchaeota in the Atacama Desert hyperarid core

10.1101/2020.07.17.208546 ◽

2020 ◽

Author(s):

Yunha Hwang ◽

Dirk Schulze-Makuch ◽

Felix L. Arens ◽

Johan S. Saenz ◽

Panagiotis S. Adam ◽

...

Keyword(s):

Nitrogen Cycling ◽

Carbon Fixation ◽

Ammonia Oxidation ◽

Bacterial Species ◽

Atacama Desert ◽

Uv Resistance ◽

Metal Transporters ◽

Carbon And Nitrogen ◽

Carbon And Nitrogen Cycling ◽

Oligotrophic Ecosystems

AbstractThe hyperarid core of the Atacama Desert is an extremely harsh environment previously thought to be colonized by only a few heterotrophic bacterial species. In addition, carbon and nitrogen cycling in these highly oligotrophic ecosystems are poorly understood. Here we genomically resolved a novel genus of Thaumarchaeota, Ca. Nitrosodesertus, found below boulders of the Atacama hyperarid core, and used comparative genomics to analyze their pangenome and site-specific adaptations. Their genomes contain genes for ammonia oxidation and the 3-hydroxypropionate/4-hydroxybutyrate carbon fixation pathway, indicating a chemolithoautotrophic lifestyle. Ca. Nitrosodesertus possesses the capacity for tolerating extensive environmental stress highlighted by the presence of genes against oxidative stress, DNA damage and genes for the formation of biofilms. These features are likely responsible for their dominance in samples with extremely low water content across three different boulder fields and eight different boulders. Genome-specific adaptations of the genomes included the presence of additional genes for UV resistance, heavy metal transporters, multiple types of ATP synthases, and divergent genes for aquaporins. Our results suggest that Thaumarchaeota mediate important carbon and nitrogen cycling in the hyperarid core of the Atacama and are part of its continuous and indigenous microbiome.

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Symbiotic bacteria of helminths: what role may they play in ecosystems under anthropogenic stress?

Journal of Helminthology ◽

10.1017/s0022149x15001066 ◽

2016 ◽

Vol 90 (6) ◽

pp. 647-657 ◽

Cited By ~ 1

Author(s):

N.J. Morley

Keyword(s):

Climate Change ◽

Environmental Stress ◽

Bacterial Communities ◽

Bacterial Species ◽

Symbiotic Bacteria ◽

Anthropogenic Pressure ◽

Anthropogenic Stress ◽

Similar Function ◽

Free Living ◽

Terrestrial Habitats

AbstractSymbiotic bacteria are a common feature of many animals, particularly invertebrates, from both aquatic and terrestrial habitats. These bacteria have increasingly been recognized as performing an important role in maintaining invertebrate health. Both ecto- and endoparasitic helminths have also been found to harbour a range of bacterial species which provide a similar function. The part symbiotic bacteria play in sustaining homeostasis of free-living invertebrates exposed to anthropogenic pressure (climate change, pollution), and the consequences to invertebrate populations when their symbionts succumb to poor environmental conditions, are increasingly important areas of research. Helminths are also susceptible to environmental stress and their symbiotic bacteria may be a key aspect of their responses to deteriorating conditions. This article summarizes the ecophysiological relationship helminths have with symbiotic bacteria and the role they play in maintaining a healthy parasite and the relevance of specific changes that occur in free-living invertebrate–bacteria interactions under anthropogenic pressure to helminths and their bacterial communities. It also discusses the importance of understanding the mechanistic sensitivity of helminth–bacteria relationships to environmental stress for comprehending the responses of parasites to challenging conditions.

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Archaea dominate oxic subseafloor communities over multimillion-year time scales

Science Advances ◽

10.1126/sciadv.aaw4108 ◽

2019 ◽

Vol 5 (6) ◽

pp. eaaw4108 ◽

Cited By ~ 24

Author(s):

Aurèle Vuillemin ◽

Scott D. Wankel ◽

Ömer K. Coskun ◽

Tobias Magritsch ◽

Sergio Vargas ◽

...

Keyword(s):

North Atlantic ◽

Organic Nitrogen ◽

Carbon Fixation ◽

Ammonia Oxidation ◽

North Atlantic Ocean ◽

Additional Energy ◽

Ammonia Oxidizing Archaea ◽

The North ◽

Metabolic Feature ◽

The North Atlantic

Ammonia-oxidizing archaea (AOA) dominate microbial communities throughout oxic subseafloor sediment deposited over millions of years in the North Atlantic Ocean. Rates of nitrification correlated with the abundance of these dominant AOA populations, whose metabolism is characterized by ammonia oxidation, mixotrophic utilization of organic nitrogen, deamination, and the energetically efficient chemolithoautotrophic hydroxypropionate/hydroxybutyrate carbon fixation cycle. These AOA thus have the potential to couple mixotrophic and chemolithoautotrophic metabolism via mixotrophic deamination of organic nitrogen, followed by oxidation of the regenerated ammonia for additional energy to fuel carbon fixation. This metabolic feature likely reduces energy loss and improves AOA fitness under energy-starved, oxic conditions, thereby allowing them to outcompete other taxa for millions of years.

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RegB/RegA, a Highly Conserved Redox-Responding Global Two-Component Regulatory System

Microbiology and Molecular Biology Reviews ◽

10.1128/mmbr.68.2.263-279.2004 ◽

2004 ◽

Vol 68 (2) ◽

pp. 263-279 ◽

Cited By ~ 125

Author(s):

Sylvie Elsen ◽

Lee R. Swem ◽

Danielle L. Swem ◽

Carl E. Bauer

Keyword(s):

Carbon Fixation ◽

Rhodobacter Capsulatus ◽

Response Regulator ◽

Bacterial Species ◽

Anaerobic Respiration ◽

Regulatory System ◽

Redox Active ◽

Membrane Bound ◽

Cognate Response Regulator ◽

Aerobic And Anaerobic

SUMMARY The Reg regulon from Rhodobacter capsulatus and Rhodobacter sphaeroides encodes proteins involved in numerous energy-generating and energy-utilizing processes such as photosynthesis, carbon fixation, nitrogen fixation, hydrogen utilization, aerobic and anaerobic respiration, denitrification, electron transport, and aerotaxis. The redox signal that is detected by the membrane-bound sensor kinase, RegB, appears to originate from the aerobic respiratory chain, given that mutations in cytochrome c oxidase result in constitutive RegB autophosphorylation. Regulation of RegB autophosphorylation also involves a redox-active cysteine that is present in the cytosolic region of RegB. Both phosphorylated and unphosphorylated forms of the cognate response regulator RegA are capable of activating or repressing a variety of genes in the regulon. Highly conserved homologues of RegB and RegA have been found in a wide number of photosynthetic and nonphotosynthetic bacteria, with evidence suggesting that RegB/RegA plays a fundamental role in the transcription of redox-regulated genes in many bacterial species.

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Genomic Characterization of VIM Metallo-β-Lactamase-Producing Alcaligenes faecalis from Gaza, Palestine

Antimicrobial Agents and Chemotherapy ◽

10.1128/aac.01499-17 ◽

2017 ◽

Vol 61 (11) ◽

Cited By ~ 5

Author(s):

Nahed Al Laham ◽

Kalyan D. Chavda ◽

Astrid V. Cienfuegos-Gallet ◽

Barry N. Kreiswirth ◽

Liang Chen

Keyword(s):

Bacterial Species ◽

Alcaligenes Faecalis ◽

Gram Negative Bacteria ◽

Sequencing Analysis ◽

Large Hospital ◽

Content Type ◽

Next Generation Sequencing Analysis ◽

Genomic Characterization ◽

Generation Sequencing

ABSTRACT Carbapenemase-producing Gram-negative bacteria (CP-GNB) have increasingly spread worldwide, and different families of carbapenemases have been identified in various bacterial species. Here, we report the identification of five VIM metallo-β-lactamase-producing Alcaligenes faecalis isolates associated with a small outbreak in a large hospital in Gaza, Palestine. Next-generation sequencing analysis showed bla VIM-2 is harbored by a chromosomal genomic island among three strains, while bla VIM-4 is carried by a novel plasmid in two strains.

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The World of Algae Reveals a Broad Variety of Cryptochrome Properties and Functions

Frontiers in Plant Science ◽

10.3389/fpls.2021.766509 ◽

2021 ◽

Vol 12 ◽

Author(s):

Jan Petersen ◽

Anxhela Rredhi ◽

Julie Szyttenholm ◽

Sabine Oldemeyer ◽

Tilman Kottke ◽

...

Keyword(s):

Carbon Fixation ◽

Algal Cell ◽

Algal Species ◽

Life Cycles ◽

Land Plants ◽

Abiotic Factor ◽

Secondary Endosymbiosis ◽

Biological Clocks ◽

Terrestrial Habitats ◽

Broad Variety

Algae are photosynthetic eukaryotic (micro-)organisms, lacking roots, leaves, and other organs that are typical for land plants. They live in freshwater, marine, or terrestrial habitats. Together with the cyanobacteria they contribute to about half of global carbon fixation. As primary producers, they are at the basis of many food webs and they are involved in biogeochemical processes. Algae are evolutionarily distinct and are derived either by primary (e.g., green and red algae) or secondary endosymbiosis (e.g., diatoms, dinoflagellates, and brown algae). Light is a key abiotic factor needed to maintain the fitness of algae as it delivers energy for photosynthesis, regulates algal cell- and life cycles, and entrains their biological clocks. However, excess light can also be harmful, especially in the ultraviolet range. Among the variety of receptors perceiving light information, the cryptochromes originally evolved as UV-A and blue-light receptors and have been found in all studied algal genomes so far. Yet, the classification, biophysical properties, wavelength range of absorbance, and biological functions of cryptochromes are remarkably diverse among algal species, especially when compared to cryptochromes from land plants or animals.

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Genome wide transcriptomic analysis of the soil ammonia oxidizing archaeon Nitrososphaera viennensis upon exposure to copper limitation

The ISME Journal ◽

10.1038/s41396-020-0715-2 ◽

2020 ◽

Vol 14 (11) ◽

pp. 2659-2674 ◽

Cited By ~ 2

Author(s):

Carolina Reyes ◽

Logan H. Hodgskiss ◽

Melina Kerou ◽

Thomas Pribasnig ◽

Sophie S. Abby ◽

...

Keyword(s):

Electron Transport ◽

Carbon Fixation ◽

Ammonia Oxidation ◽

Transcriptomic Analysis ◽

Sequence Motifs ◽

Conserved Sequence ◽

Model Soil ◽

Ammonia Oxidizing Archaea ◽

Nitrite Production ◽

Cu Uptake

Abstract Ammonia-oxidizing archaea (AOA) are widespread in nature and are involved in nitrification, an essential process in the global nitrogen cycle. The enzymes for ammonia oxidation and electron transport rely heavily on copper (Cu), which can be limited in nature. In this study the model soil archaeon Nitrososphaera viennensis was investigated via transcriptomic analysis to gain insight regarding possible Cu uptake mechanisms and compensation strategies when Cu becomes limiting. Upon Cu limitation, N. viennensis exhibited impaired nitrite production and thus growth, which was paralleled by downregulation of ammonia oxidation, electron transport, carbon fixation, nucleotide, and lipid biosynthesis pathway genes. Under Cu-limitation, 1547 out of 3180 detected genes were differentially expressed, with 784 genes upregulated and 763 downregulated. The most highly upregulated genes encoded proteins with a possible role in Cu binding and uptake, such as the Cu chelator and transporter CopC/D, disulfide bond oxidoreductase D (dsbD), and multicopper oxidases. While this response differs from the marine strain Nitrosopumilus maritimus, conserved sequence motifs in some of the Cu-responsive genes suggest conserved transcriptional regulation in terrestrial AOA. This study provides possible gene regulation and energy conservation mechanisms linked to Cu bioavailability and presents the first model for Cu uptake by a soil AOA.

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Identifying and quantifying radiation damage at the atomic level

Journal of Synchrotron Radiation ◽

10.1107/s1600577515002131 ◽

2015 ◽

Vol 22 (2) ◽

pp. 201-212 ◽

Cited By ~ 35

Author(s):

Markus Gerstel ◽

Charlotte M. Deane ◽

Elspeth F. Garman

Keyword(s):

Radiation Damage ◽

Disulfide Bonds ◽

Solvent Accessibility ◽

Global Radiation ◽

Protein Structures ◽

Large Set ◽

Damage Site ◽

Site Specific ◽

Statistical Survey ◽

And Function

Radiation damage impedes macromolecular diffraction experiments. Alongside the well known effects of global radiation damage, site-specific radiation damage affects data quality and the veracity of biological conclusions on protein mechanism and function. Site-specific radiation damage follows a relatively predetermined pattern, in that different structural motifs are affected at different dose regimes: in metal-free proteins, disulfide bonds tend to break first followed by the decarboxylation of aspartic and glutamic acids. Even within these damage motifs the decay does not progress uniformly at equal rates. Within the same protein, radiation-induced electron density decay of a particular chemical group is faster than for the same group elsewhere in the protein: an effect known as preferential specific damage. Here,BDamage, a new atomic metric, is defined and validated to recognize protein regions susceptible to specific damage and to quantify the damage at these sites. By applyingBDamageto a large set of known protein structures in a statistical survey, correlations between the rates of damage and various physicochemical parameters were identified. Results indicate that specific radiation damage is independent of secondary protein structure. Different disulfide bond groups (spiral, hook, and staple) show dissimilar radiation damage susceptibility. There is a consistent positive correlation between specific damage and solvent accessibility.

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A Mesophilic, Autotrophic, Ammonia-Oxidizing Archaeon of Thaumarchaeal Group I.1a Cultivated from a Deep Oligotrophic Soil Horizon

Applied and Environmental Microbiology ◽

10.1128/aem.03730-13 ◽

2014 ◽

Vol 80 (12) ◽

pp. 3645-3655 ◽

Cited By ~ 46

Author(s):

Man-Young Jung ◽

Soo-Je Park ◽

So-Jeong Kim ◽

Jong-Geol Kim ◽

Jaap S. Sinninghe Damsté ◽

...

Keyword(s):

Carbon Fixation ◽

Ammonia Oxidation ◽

Soil Horizon ◽

Ammonia Oxidizer ◽

Rrna Gene ◽

Soil Nitrification ◽

Content Type ◽

Niche Adaptation ◽

Group I ◽

Terrestrial Environments

ABSTRACTSoil nitrification plays an important role in the reduction of soil fertility and in nitrate enrichment of groundwater. Various ammonia-oxidizing archaea (AOA) are considered to be members of the pool of ammonia-oxidizing microorganisms in soil. This study reports the discovery of a chemolithoautotrophic ammonia oxidizer that belongs to a distinct clade of nonmarine thaumarchaeal group I.1a, which is widespread in terrestrial environments. The archaeal strain MY2 was cultivated from a deep oligotrophic soil horizon. The similarity of the 16S rRNA gene sequence of strain MY2 to those of other cultivated group I.1a thaumarchaeota members, i.e.,Nitrosopumilus maritimusand “CandidatusNitrosoarchaeum koreensis,” is 92.9% for both species. Extensive growth assays showed that strain MY2 is chemolithoautotrophic, mesophilic (optimum temperature, 30°C), and neutrophilic (optimum pH, 7 to 7.5). The accumulation of nitrite above 1 mM inhibited ammonia oxidation, while ammonia oxidation itself was not inhibited in the presence of up to 5 mM ammonia. The genome size of strain MY2 was 1.76 Mb, similar to those ofN. maritimusand “Ca. Nitrosoarchaeum koreensis,” and the repertoire of genes required for ammonia oxidation and carbon fixation in thaumarchaeal group I.1a was conserved. A high level of representation of conserved orthologous genes for signal transduction and motility in the noncore genome might be implicated in niche adaptation by strain MY2. On the basis of phenotypic, phylogenetic, and genomic characteristics, we propose the name “CandidatusNitrosotenuis chungbukensis” for the ammonia-oxidizing archaeal strain MY2.

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The direct interaction of NME3 with Tip60 in DNA repair

Biochemical Journal ◽

10.1042/bcj20160122 ◽

2016 ◽

Vol 473 (9) ◽

pp. 1237-1245 ◽

Cited By ~ 12

Author(s):

Ning Tsao ◽

Ya-Chi Yang ◽

Yu-Jyun Deng ◽

Zee-Fen Chang

Keyword(s):

Dna Damage ◽

Dna Repair ◽

Direct Interaction ◽

Ndp Kinase ◽

Damage Site ◽

Site Specific ◽

Catalytic Function ◽

Repair Efficiency ◽

Subsequent Step ◽

Dna Replication And Repair

Cellular supply of dNTPs via RNR (ribonucleotide reductase) is crucial for DNA replication and repair. It has been shown that DNA-damage-site-specific recruitment of RNR is critical for DNA repair efficiency in quiescent cells. The catalytic function of RNR produces dNDPs. The subsequent step of dNTP formation requires the function of NDP kinase. There are ten isoforms of NDP kinase in human cells. In the present study, we identified NME3 as one specific NDP kinase that interacts directly with Tip60, a histone acetyltransferase, to form a complex with RNR. Our data reveal that NME3 recruitment to DNA damage sites depends on this interaction. Disruption of interaction of NME3 with Tip60 suppressed DNA repair in serum-deprived cells. Thus Tip60 interacts with RNR and NME3 to provide site-specific synthesis of dNTP for facilitating DNA repair in serum-deprived cells which contain low levels of dNTPs.

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