Proteolytic systems of archaea: slicing, dicing, and mincing in the extreme

Maupin-Furlow, Julie A.

doi:10.1042/etls20180025

Cited by 9 publications

(6 citation statements)

References 201 publications

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“…None of these peptidases are classified into groups known to be exported to the extracellular space (Maupin-Furlow 2018 ) and correspondingly, SignalP 5.0 (Almagro Armenteros et al 2019 ) only identified export signal peptides in seven sequences in total. These are the M14 carboxypeptidase of MAG011 (also annotated in MAG060 and MAG107), the S08 endopeptidase of MAG011 (also detected in MAG019 and MAG107), both G01 endopeptidases in MAG033 and MAG097, the S12 D-Ala/D-Ala carboxypeptidase of MAG097 (three copies detected in MAG107), signal peptidase S26 of MAG117 (found in multiple MAGs, see supplementary tables), and the rhomboid peptidase S54 of MAG125 (detected in all MAGs, except MAG095, MAG107 and MAG121).…”

Section: Resultsmentioning

confidence: 99%

The Polar Fox Lagoon in Siberia harbours a community of Bathyarchaeota possessing the potential for peptide fermentation and acetogenesis

Berben

Bó

Zandt

et al. 2022

Antonie van Leeuwenhoek

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Archaea belonging to the phylum Bathyarchaeota are the predominant archaeal species in cold, anoxic marine sediments and additionally occur in a variety of habitats, both natural and man-made. Metagenomic and single-cell sequencing studies suggest that Bathyarchaeota may have a significant impact on the emissions of greenhouse gases into the atmosphere, either through direct production of methane or through the degradation of complex organic matter that can subsequently be converted into methane. This is especially relevant in permafrost regions where climate change leads to thawing of permafrost, making high amounts of stored carbon bioavailable. Here we present the analysis of nineteen draft genomes recovered from a sediment core metagenome of the Polar Fox Lagoon, a thermokarst lake located on the Bykovsky Peninsula in Siberia, Russia, which is connected to the brackish Tiksi Bay. We show that the Bathyarchaeota in this lake are predominantly peptide degraders, producing reduced ferredoxin from the fermentation of peptides, while degradation pathways for plant-derived polymers were found to be incomplete. Several genomes encoded the potential for acetogenesis through the Wood-Ljungdahl pathway, but methanogenesis was determined to be unlikely due to the lack of genes encoding the key enzyme in methanogenesis, methyl-CoM reductase. Many genomes lacked a clear pathway for recycling reduced ferredoxin. Hydrogen metabolism was also hardly found: one type 4e [NiFe] hydrogenase was annotated in a single MAG and no [FeFe] hydrogenases were detected. Little evidence was found for syntrophy through formate or direct interspecies electron transfer, leaving a significant gap in our understanding of the metabolism of these organisms.

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Section: Resultsmentioning

confidence: 99%

The Polar Fox Lagoon in Siberia harbours a community of Bathyarchaeota possessing the potential for peptide fermentation and acetogenesis

Berben

Bó

Zandt

et al. 2022

Antonie van Leeuwenhoek

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“…5 ) as well as pathways for amino acid utilization [ 81 , 82 ]. However, these methanogenic archaea and anaerobic methanotrophs rely on methanogenesis or methanotrophy, respectively, while using amino acids for protein biosynthesis [ 83 ], for cell wall rearrangement during cell growth [ 84 , 85 ], or uptake of certain amino acids as osmolytes [ 86 ]. Another explanation for the inactive MBG-D archaea might be their extremely low growth rate [ 20 ].…”

Section: Discussionmentioning

confidence: 99%

Catabolic protein degradation in marine sediments confined to distinct archaea

et al. 2022

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Metagenomic analysis has facilitated prediction of a variety of carbon utilization potentials by uncultivated archaea including degradation of protein, which is a wide-spread carbon polymer in marine sediments. However, the activity of detrital catabolic protein degradation is mostly unknown for the vast majority of archaea. Here, we show actively executed protein catabolism in three archaeal phyla (uncultivated Thermoplasmata, SG8-5; Bathyarchaeota subgroup 15; Lokiarchaeota subgroup 2c) by RNA- and lipid-stable isotope probing in incubations with different marine sediments. However, highly abundant potential protein degraders Thermoprofundales (MBG-D) and Lokiarchaeota subgroup 3 were not incorporating 13C-label from protein during incubations. Nonetheless, we found that the pathway for protein utilization was present in metagenome associated genomes (MAGs) of active and inactive archaea. This finding was supported by screening extracellular peptidases in 180 archaeal MAGs, which appeared to be widespread but not correlated to organisms actively executing this process in our incubations. Thus, our results have important implications: (i) multiple low-abundant archaeal groups are actually catabolic protein degraders; (ii) the functional role of widespread extracellular peptidases is not an optimal tool to identify protein catabolism, and (iii) catabolic degradation of sedimentary protein is not a common feature of the abundant archaeal community in temperate and permanently cold marine sediments.

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“…identity), Thermoplasma volcanium (70.7%), T. acidophilum (69.1%) and other archaea from the order Thermoplasmatales without taxonomic status (e.g., Thermoplasmatales "E-" and "A-plasma"). These proteolytic membrane-associated proteins are also known to occur in diverse archaea [23]. However, it must be noted that this protein has one of the lowest abundances in the proteome, only 0.001% in the cold and 0.015% under optimal growth conditions.…”

Section: Proteins Expressed Under Optimal Growth Conditionsmentioning

confidence: 99%

Proteome Cold-Shock Response in the Extremely Acidophilic Archaeon, Cuniculiplasma divulgatum

et al. 2020

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The archaeon Cuniculiplasma divulgatum is ubiquitous in acidic environments with low-to-moderate temperatures. However, molecular mechanisms underlying its ability to thrive at lower temperatures remain unexplored. Using mass spectrometry (MS)-based proteomics, we analysed the effect of short-term (3 h) exposure to cold. The C. divulgatum genome encodes 2016 protein-coding genes, from which 819 proteins were identified in the cells grown under optimal conditions. In line with the peptidolytic lifestyle of C. divulgatum, its intracellular proteome revealed the abundance of proteases, ABC transporters and cytochrome C oxidase. From 747 quantifiable polypeptides, the levels of 582 proteins showed no change after the cold shock, whereas 104 proteins were upregulated suggesting that they might be contributing to cold adaptation. The highest increase in expression appeared in low-abundance (0.001–0.005 fmol%) proteins for polypeptides’ hydrolysis (metal-dependent hydrolase), oxidation of amino acids (FAD-dependent oxidoreductase), pyrimidine biosynthesis (aspartate carbamoyltransferase regulatory chain proteins), citrate cycle (2-oxoacid ferredoxin oxidoreductase) and ATP production (V type ATP synthase). Importantly, the cold shock induced a substantial increase (6% and 9%) in expression of the most-abundant proteins, thermosome beta subunit and glutamate dehydrogenase. This study has outlined potential mechanisms of environmental fitness of Cuniculiplasma spp. allowing them to colonise acidic settings at low/moderate temperatures.

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Proteolytic systems of archaea: slicing, dicing, and mincing in the extreme

Cited by 9 publications

References 201 publications

The Polar Fox Lagoon in Siberia harbours a community of Bathyarchaeota possessing the potential for peptide fermentation and acetogenesis

The Polar Fox Lagoon in Siberia harbours a community of Bathyarchaeota possessing the potential for peptide fermentation and acetogenesis

Catabolic protein degradation in marine sediments confined to distinct archaea

Proteome Cold-Shock Response in the Extremely Acidophilic Archaeon, Cuniculiplasma divulgatum

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