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Exploration of the Types of Rarity in the Arctic Ocean from the Perspective of Multiple Methodologies

  • Environmental Microbiology
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Abstract

The Arctic Ocean is facing rapid environmental changes with cascading effects on the entire Arctic marine ecosystem. However, we have a limited understanding of the consequences such changes have on bacteria and archaea (prokaryotes) at the base of the marine food web. In this study, we show how the prokaryotic rare biosphere behaves over a range of highly heterogeneous environmental conditions using 16S rRNA gene reads from amplicon and metagenome sequencing data from seawater samples collected during the Norwegian young sea ICE expedition between late winter and early summer. The prokaryotic rare biosphere was analyzed using different approaches: amplicon sequence variants and operational taxonomic units from the 16S rRNA gene amplicons and operational taxonomic units from the 16S rRNA genes of the metagenomes. We found that prokaryotic rare biosphere communities are specific to certain water masses, and that the majority of the rare taxa identified were always rare and disappeared in at least one sample under changing conditions, suggesting their high sensitivity to environmental heterogeneity. In addition, our methodological comparison revealed a good performance of 16S rRNA gene amplicon sequencing in describing rare biosphere patterns, while the metagenome-derived data were better to capture a significant diversity of so-far uncultivated rare taxa. Our analysis on the dynamics of the rare prokaryotic biosphere, by combining different methodological approaches, improves the description of the types of rarity predicted from Community Assembly theory in the Arctic Ocean.

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Data availability

The raw sequences used for 16S rRNA gene analysis and metagenomes are publically available at the European Nucleotide Archive (ENA) under the accession numbers PRJEB21950 and PRJEB15043. The sample vs. 16S rRNA gene–derived OTUs table is available in the MGnify platform (Study: MGYS00001922). The sample versus metagenomic-derived OTUs (mOTU) table is available at the MGnify platform (Study: MGYS00001869).

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Code availability

The code used for processing of raw 16S rRNA gene sequences into ASVs and the code for the diversity metrics used for all datasets (ASVs, OTUs, and mOTUs) are available in a single R script (Supplementary Data S1). Custom commands were used for the Circos figures, based on the data obtained from the R script provided.

Funding

The Portuguese Science and Technology Foundation (FCT) funded this study through the grants PTDC/CTA-AMB/30997/2017 and PTDC/CTA-AMB/4946/2020 to C.M., 2020.03139 CEECIND to C.M., and the PhD grant 2020.04453.BD to F.P. Further Arctic campaign logistic and traveling support was provided by the Portuguese Polar Program (PROPOLAR) and by the former Centre for Ice, Climate and Ecosystems at the Norwegian Polar Institute, the Research Council of Norway (project no. 244646), the Norwegian Ministries of Foreign Affairs and Climate and Environment through the program Arktis 2030 (project ID Arctic). This study was also partially funded by “Programa Operacional Regional de Lisboa” (Project N. 007317) and the Strategic Funding UIDB/04423/2020, UIDP/04565/2020, and UIDB/04565/2020 through national funds provided by FCT and European Regional Development Fund (ERDF), in the framework of the “PT2020” program.

Author information

Authors and Affiliations

  1. Interdisciplinary Centre of Marine and Environmental Research (CIIMAR), University of Porto, Porto, Portugal

    Francisco Pascoal & Catarina Magalhães

  2. Faculty of Sciences, University of Porto, Porto, Portugal

    Francisco Pascoal & Catarina Magalhães

  3. Department of Bioengineering, Institute for Bioengineering and Biosciences (iBB), Instituto Superior Técnico, University of Lisbon, Lisbon, Portugal

    Rodrigo Costa

  4. Centre of Marine Sciences (CCMAR), University of Algarve, Faro, Portugal

    Rodrigo Costa

  5. U.S. Department of Energy Joint Genome Institute, Berkeley, CA, USA

    Rodrigo Costa

  6. Environmental Genomics and Systems Biology Division, Lawrence Berkeley National Laboratory, Berkeley, CA, USA

    Rodrigo Costa

  7. Norwegian Polar Institute, Fram Centre, N-9296, Tromsø, Norway

    Philipp Assmy & Pedro Duarte

  8. School of Science & Engineering, University of Waikato, Hamilton, New Zealand

    Catarina Magalhães

  9. Ocean Frontier Institute, Dalhousie University, Halifax, NS, Canada

    Catarina Magalhães

Authors
  1. Francisco Pascoal
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  2. Rodrigo Costa
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  3. Philipp Assmy
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  4. Pedro Duarte
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  5. Catarina Magalhães
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Contributions

F.P., R.C., and C.M. conceptualized the manuscript. F.P. wrote the R code for all figures and tables and designed the Circos figures. F.P .wrote and R.C., C.M., P.A., and P.D. reviewed the first manuscript draft. C.M. and P.D. designed the sampling campaign. C.M., R.C., and P.A. funded the work. All authors reviewed, improved, and approved the final version of the manuscript.

Corresponding author

Correspondence to Francisco Pascoal.

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The authors declare no competing interests.

Supplementary Information

Supplementary Fig. S1

Quality scores profile for the forward 16S rRNA gene sequences (PNG 6307 kb)

High Resolution image (TIFF 5265 kb)

Supplementary Fig. S2

Quality scores profile for the reverse 16S rRNA gene sequences (PNG 6497 kb)

High Resolution image (TIFF 4995 kb)

Supplementary Fig. S3

MultiCoLA results of Procrustes and boxplot with the relative abundance equivalent of the selected cutoff, for non-rarefied data; a Procrustes results for the ASVs; b boxplots with relative abundance equivalent for each sample, after application of the selected threshold, for the ASVs; c Procrustes results for the OTUs; d boxplots with relative abundance equivalent for each sample, after application of the selected threshold, for the OTUs; e Procrustes results for the mOTUs; f boxplots with relative abundance equivalent for each sample, after application of the selected threshold, for the mOTUs (PNG 1425 kb)

Supplementary Fig. S4

MultiCoLA results of Procrustes for rarefied data. a Procrustes results for the ASVs; b Procrustes results for the OTUs; c Procrustes results for the mOTUs (PNG 323 kb)

Supplementary Fig. S5

a Rarefaction curve for ASV samples; b rarefaction curve for OTU samples; c rarefaction curves for mOTU samples (PNG 838 kb)

Supplementary Fig. S6

Alpha diversity for the total community (rarefied) and for the rare biosphere, defined by the MultiCoLA algorithm, across ASVs, OTUs, and mOTUs. a Number of sequences for the total community and b for the rare biosphere; c species richness for the total community and d rare biosphere; e Shannon equitability for the total community and f rare biosphere (PNG 583 kb)

Supplementary Fig. S7

Alpha diversity for the total community (non-rarefied) and for the rare biosphere, defined by the 0.1% relative abundance threshold, per sample, across ASVs, OTUs, and mOTUs. a Number of sequences for the total community and b for the rare biosphere; c species richness for the total community and d rare biosphere; e Shannon equitability for the total community and f rare biosphere (PNG 587 kb)

Supplementary Fig. S8

Alpha diversity for the total community (rarefied) and for the rare biosphere, defined by defined by the 0.1% relative abundance threshold, per sample, across ASVs, OTUs, and mOTUs. a Number of sequences for the total community and b for the rare biosphere; c species richness for the total community and d rare biosphere; e Shannon equitability for the total community and f rare biosphere (PNG 581 kb)

Supplementary Fig. S9

Dendrograms and multivariate analysis for the rare biosphere, defined by MultiCoLA and rarefied. a Dendrogram of the rare ASVs; b dendrogram of the rare OTUs; c dendrogram of the rare mOTUs; d CA for the rare ASVs; e CA for the rare OTUs; f CA for the rare mOTUs (PNG 1200 kb)

Supplementary Fig. S10

Dendrograms and multivariate analysis for the rare biosphere, defined by 0.1% relative abundance threshold, per sample, and non-rarefied. a Dendrogram of the rare ASVs; b dendrogram of the rare OTUs; c dendrogram of the rare mOTUs; d CA for the rare ASVs; e CA for the rare OTUs; f CA for the rare mOTUs (PNG 1187 kb)

Supplementary Fig. S11

Dendrograms and multivariate analysis for the rare biosphere, defined by 0.1% relative abundance threshold, per sample, and rarefied. a Dendrogram of the rare ASVs; b Dendrogram of the rare OTUs; c Dendrogram of the rare mOTUs; d CA for the rare ASVs; e CA for the rare OTUs; f CA for the rare mOTUs (PNG 1186 kb)

Supplementary Fig. S12

Stacked bar plots with the proportion of taxa for each type of rarity, if rare, and for the proportion of abundant taxa. Rare biosphere was defined by the MultiCoLA algorithm, from rarefied data. a The proportions for the rare ASVs; b the proportions for the rare OTUs; c the proportions for the rare mOTUs. The stacked bar plots are colored with purple for transiently rare taxa (TRT), blue for permanently rare taxa (PRT), green for conditionally rare taxa (CRT), and red for the abundant taxa. Within each dataset, different groups of samples were selected, specifically: “All” is for all samples; “March” is the group of samples from the month of March and they represent different depths (5, 50, and 250 m); “April” is the group of samples from the month of April and they represent different depths (5, 50, and 250 m); “June” is the group of samples from the month of June and they represent different depths (5, 20, and 250 m); “5m” is the group of samples taken at 5 m of depth and they represent the different months (March, April, and June); “20m or 50m” is the group of samples taken at 20 or 50 m of depth and they represent the different months (March, April, and June); “250m” is the group of samples taken at 250 m of depth and they represent the different months (March, April, and June) (PNG 260 kb)

Supplementary Fig. S13

Stacked bar plots with the proportion of taxa for each type of rarity, if rare, and for the proportion of abundant taxa. Rare biosphere was defined by the 0.1% relative abundance threshold, per sample, from non-rarefied data. a The proportions for the rare ASVs; b the proportions for the rare OTUs; c the proportions for the rare mOTUs. The stacked bar plots are colored with purple for transiently rare taxa (TRT), blue for permanently rare taxa (PRT), green for conditionally rare taxa (CRT), and red for the abundant taxa. Within each dataset, different groups of samples were selected, specifically: “All” is for all samples; “March” is the group of samples from the month of March and they represent different depths (5, 50, and 250 m); “April” is the group of samples from the month of April and they represent different depths (5, 50, and 250 m); “June” is the group of samples from the month of June and they represent different depths (5, 20, and 250 m); “5m” is the group of samples taken at 5 m of depth and they represent the different months (March, April, and June); “20m or 50m” is the group of samples taken at 20 or 50 m of depth and they represent the different months (March, April, and June); “250m” is the group of samples taken at 250 m of depth and they represent the different months (March, April, and June) (PNG 260 kb)

Supplementary Fig. S14

Stacked bar plots with the proportion of taxa for each type of rarity, if rare, and for the proportion of abundant taxa. Rare biosphere was defined by the 0.1% relative abundance threshold, per sample, from rarefied data. a The proportions for the rare ASVs; b the proportions for the rare OTUs; c the proportions for the rare mOTUs. The stacked bar plots are colored with purple for transiently rare taxa (TRT), blue for permanently rare taxa (PRT), green for conditionally rare taxa (CRT), and red for the abundant taxa. Within each dataset, different groups of samples were selected, specifically: “All” is for all samples; “March” is the group of samples from the month of March and they represent different depths (5, 50, and 250 m); “April” is the group of samples from the month of April and they represent different depths (5, 50, and 250 m); “June” is the group of samples from the month of June and they represent different depths (5, 20, and 250 m); “5m” is the group of samples taken at 5 m of depth and they represent the different months (March, April, and June); “20m or 50m” is the group of samples taken at 20 or 50 m of depth and they represent the different months (March, April, and June); “250m” is the group of samples taken at 250 m of depth and they represent the different months (March, April, and June) (PNG 263 kb)

Supplementary Data S1

Text file with the R code used for the processing of raw 16S rRNA gene sequences into ASVs and for the diversity metrics used for all datasets: ASVs, OTUs, and mOTUs (R 178 kb)

Supplementary Table S1

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Pascoal, F., Costa, R., Assmy, P. et al. Exploration of the Types of Rarity in the Arctic Ocean from the Perspective of Multiple Methodologies. Microb Ecol 84, 59–72 (2022). https://doi.org/10.1007/s00248-021-01821-9

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  • DOI: https://doi.org/10.1007/s00248-021-01821-9

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