Functional and Taxonomic Diversity of Anaerobes in Supraglacial Microbial Communities

Recent evidence disclosed the presence of a potential niche for anaerobic microorganisms and anaerobic processes in supraglacial sediments (cryoconite), but a detailed description of the structure and functions of the anaerobic population is still lacking. This work used rRNA and mRNA sequencing and demonstrated that anaerobes are very active in these environments and represent a relevant albeit neglected part of the ecosystem functions in these environments. ABSTRACT Cryoconite holes are small ponds present on the surface of most glaciers filled with meltwater and sediment at the bottom. Although they are characterized by extreme conditions, they host bacterial communities with high taxonomic and functional biodiversity. Despite that evidence for a potential niche for anaerobic microorganisms and anaerobic processes has recently emerged, the composition of the microbial communities of the cryoconite reported so far has not shown the relevant presence of anaerobic taxa. We hypothesize that this is due to the lower growth yield of anaerobes compared to aerobic microorganisms. In this work, we aim at evaluating whether the anaerobic bacterial community represents a relevant fraction of the biodiversity of the cryoconite and at describing its structure and functions. We collected sediment samples from cryoconite holes on the Forni Glacier (Italy) and sequenced both 16S rRNA amplicon genes and 16S rRNA amplicon transcripts at different times of the day along a clear summer day. Results showed that a relevant fraction of taxa has been detected only by 16S rRNA transcripts and was undetectable in 16S rRNA gene amplicons. Furthermore, in the transcript approach, anaerobic taxa were overrepresented compared with DNA sequencing. The metatranscriptomics approach was used also to investigate the expression of the main metabolic functions. Results showed the occurrence of syntrophic and commensalism relationships among fermentative bacteria, hydrogenothrophs, and consumers of fermentation end products, which have never been reported so far in cryoconite. IMPORTANCE Recent evidence disclosed the presence of a potential niche for anaerobic microorganisms and anaerobic processes in supraglacial sediments (cryoconite), but a detailed description of the structure and functions of the anaerobic population is still lacking. This work used rRNA and mRNA sequencing and demonstrated that anaerobes are very active in these environments and represent a relevant albeit neglected part of the ecosystem functions in these environments.

[1]  R. Ambrosini,et al.  Trophic and symbiotic links between obligate-glacier water bears (Tardigrada) and cryoconite microorganisms , 2022, PloS one.

[2]  Keshao Liu,et al.  Snowstorm Enhanced the Deterministic Processes of the Microbial Community in Cryoconite at Laohugou Glacier, Tibetan Plateau , 2022, Frontiers in Microbiology.

[3]  R. Ambrosini,et al.  Is Oxygenation Related to the Decomposition of Organic Matter in Cryoconite Holes? , 2021, Ecosystems.

[4]  J. Priscu,et al.  Glacial Ecosystems , 2021 .

[5]  H. Satoh,et al.  Redox stratification within cryoconite granules influences the nitrogen cycle on glaciers. , 2020, FEMS microbiology ecology.

[6]  A. Anesio,et al.  Physiological Capabilities of Cryoconite Hole Microorganisms , 2020, Frontiers in Microbiology.

[7]  J. Izopet,et al.  Insertions and Duplications in the Polyproline Region of the Hepatitis E Virus , 2020, Frontiers in Microbiology.

[8]  R. Ambrosini,et al.  Water bears dominated cryoconite hole ecosystems: densities, habitat preferences and physiological adaptations of Tardigrada on an alpine glacier , 2019, Aquatic Ecology.

[9]  R. Ambrosini,et al.  Bacterial communities of cryoconite holes of a temperate alpine glacier show both seasonal trends and year-to-year variability , 2018, Annals of Glaciology.

[10]  U. Ijaz,et al.  The active microbial community more accurately reflects the anaerobic digestion process: 16S rRNA (gene) sequencing as a predictive tool , 2018, Microbiome.

[11]  A. Doxey,et al.  Aerobic proteobacterial methylotrophs in Movile Cave: genomic and metagenomic analyses , 2018, Microbiome.

[12]  A. Anesio,et al.  Rapid development of anoxic niches in supraglacial ecosystems , 2018 .

[13]  Sota Tanaka,et al.  Biogeography of cryoconite forming cyanobacteria on polar and Asian glaciers , 2017 .

[14]  R. Ambrosini,et al.  Temporal variability of bacterial communities in cryoconite on an alpine glacier , 2017, Environmental microbiology reports.

[15]  R. Ambrosini,et al.  Potential sources of bacteria colonizing the cryoconite of an Alpine glacier , 2017, PloS one.

[16]  P. Legendre,et al.  Ecologically meaningful transformations for ordination of species data , 2001, Oecologia.

[17]  C. Mayer,et al.  Diversity and Assembling Processes of Bacterial Communities in Cryoconite Holes of a Karakoram Glacier , 2017, Microbial Ecology.

[18]  R. Gromadka,et al.  Enrichment of Cryoconite Hole Anaerobes: Implications for the Subglacial Microbiome , 2016, Microbial Ecology.

[19]  Paul J. McMurdie,et al.  DADA2: High resolution sample inference from Illumina amplicon data , 2016, Nature Methods.

[20]  C. Mayer,et al.  Light-dependent microbial metabolisms drive carbon fluxes on glacier surfaces , 2016, The ISME Journal.

[21]  N. Takeuchi,et al.  Cryoconite: The dark biological secret of the cryosphere , 2016 .

[22]  M. Koblížek Ecology of aerobic anoxygenic phototrophs in aquatic environments. , 2015, FEMS microbiology reviews.

[23]  A. Boetius,et al.  Microbial ecology of the cryosphere: sea ice and glacial habitats , 2015, Nature Reviews Microbiology.

[24]  M. Galan,et al.  A Comparison between Transcriptome Sequencing and 16S Metagenomics for Detection of Bacterial Pathogens in Wildlife , 2015, PLoS neglected tropical diseases.

[25]  L. Hansen,et al.  Different bulk and active bacterial communities in cryoconite from the margin and interior of the Greenland ice sheet. , 2015, Environmental microbiology reports.

[26]  S. Ishii,et al.  The nitrogen cycle in cryoconites: naturally occurring nitrification-denitrification granules on a glacier. , 2014, Environmental microbiology.

[27]  Gaiyun Zhang,et al.  Diversity and novelty of actinobacteria in Arctic marine sediments , 2014, Antonie van Leeuwenhoek.

[28]  C. Kellogg,et al.  Comparison of DNA preservation methods for environmental bacterial community samples. , 2013, FEMS microbiology ecology.

[29]  M. Stibal,et al.  Biological processes on glacier and ice sheet surfaces , 2012 .

[30]  Siu-Ming Yiu,et al.  IDBA-UD: a de novo assembler for single-cell and metagenomic sequencing data with highly uneven depth , 2012, Bioinform..

[31]  Andrew G. Fountain,et al.  The Disappearing Cryosphere: Impacts and Ecosystem Responses to Rapid Cryosphere Loss , 2012 .

[32]  Steven L Salzberg,et al.  Fast gapped-read alignment with Bowtie 2 , 2012, Nature Methods.

[33]  Adam M. Phillippy,et al.  Interactive metagenomic visualization in a Web browser , 2011, BMC Bioinformatics.

[34]  S. Schuster,et al.  Integrative analysis of environmental sequences using MEGAN4. , 2011, Genome research.

[35]  S. K. Schmidt,et al.  Global Distribution of Polaromonas Phylotypes - Evidence for a Highly Successful Dispersal Capacity , 2011, PloS one.

[36]  Alexandre M. Anesio,et al.  Carbon fluxes through bacterial communities on glacier surfaces , 2010, Annals of Glaciology.

[37]  Miquel De Cáceres,et al.  Improving indicator species analysis by combining groups of sites , 2010 .

[38]  Aaron R. Quinlan,et al.  Bioinformatics Applications Note Genome Analysis Bedtools: a Flexible Suite of Utilities for Comparing Genomic Features , 2022 .

[39]  Miriam L. Land,et al.  Trace: Tennessee Research and Creative Exchange Prodigal: Prokaryotic Gene Recognition and Translation Initiation Site Identification Recommended Citation Prodigal: Prokaryotic Gene Recognition and Translation Initiation Site Identification , 2022 .

[40]  D. Sofrová Sulfur Metabolism in Phototrophic Organisms , 2009, Biologia Plantarum.

[41]  Gonçalo R. Abecasis,et al.  The Sequence Alignment/Map format and SAMtools , 2009, Bioinform..

[42]  Georges N. Cohen,et al.  “Candidatus Cloacamonas Acidaminovorans”: Genome Sequence Reconstruction Provides a First Glimpse of a New Bacterial Division , 2008, Journal of bacteriology.

[43]  R. Hell,et al.  Sulfur Metabolism in Phototrophic Organisms , 2008 .

[44]  J. Tiedje,et al.  Naïve Bayesian Classifier for Rapid Assignment of rRNA Sequences into the New Bacterial Taxonomy , 2007, Applied and Environmental Microbiology.

[45]  M. Yakimov,et al.  Study of bacterial communities in Antarctic coastal waters by a combination of 16S rRNA and 16S rDNA sequencing. , 2006, Environmental microbiology.

[46]  M. Höfle,et al.  Composition and Dynamics of Bacterial Communities of a Drinking Water Supply System as Assessed by RNA- and DNA-Based 16S rRNA Gene Fingerprinting , 2006, Applied and Environmental Microbiology.

[47]  Sang Joon Kim,et al.  A Mathematical Theory of Communication , 2006 .

[48]  J. Reeve,et al.  Molecular identification of Bacteria and Eukarya inhabiting an Antarctic cryoconite hole , 2003, Extremophiles.

[49]  F. Schinner,et al.  Characterization of Heterotrophic Microorganisms in Alpine Glacier Cryoconite , 2002 .

[50]  Y. Benjamini,et al.  THE CONTROL OF THE FALSE DISCOVERY RATE IN MULTIPLE TESTING UNDER DEPENDENCY , 2001 .

[51]  R. Amann,et al.  Combined Use of 16S Ribosomal DNA and 16S rRNA To Study the Bacterial Community of Polychlorinated Biphenyl-Polluted Soil , 2001, Applied and Environmental Microbiology.

[52]  Susumu Goto,et al.  KEGG: Kyoto Encyclopedia of Genes and Genomes , 2000, Nucleic Acids Res..

[53]  S. Tseng,et al.  Treatment of monosodium glutamate fermentation wastewater with anaerobic biological fluidized bed process. , 1990 .

[54]  B. Capdeville,et al.  Kinetics and Modelling of Aerobic and Anaerobic Film Growth , 1990 .

[55]  C. Gini Variabilità e mutabilità : contributo allo studio delle distribuzioni e delle relazioni statistiche , 1912 .