PCR Biases Distort Bacterial and Archaeal Community Structure in Pyrosequencing Datasets
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{"title"=>"PCR biases distort bacterial and archaeal community structure in pyrosequencing datasets", "type"=>"journal", "authors"=>[{"first_name"=>"Ameet J.", "last_name"=>"Pinto", "scopus_author_id"=>"55314883000"}, {"first_name"=>"Lutgarde", "last_name"=>"Raskin", "scopus_author_id"=>"7005962087"}], "year"=>2012, "source"=>"PLoS ONE", "identifiers"=>{"doi"=>"10.1371/journal.pone.0043093", "sgr"=>"84865060813", "issn"=>"19326203", "pui"=>"365445653", "isbn"=>"1932-6203 (Electronic)\\r1932-6203 (Linking)", "pmid"=>"22905208", "scopus"=>"2-s2.0-84865060813"}, "id"=>"90dc7e03-8f0c-3679-a47d-66d6a2a4e8c3", "abstract"=>"As 16S rRNA gene targeted massively parallel sequencing has become a common tool for microbial diversity investigations, numerous advances have been made to minimize the influence of sequencing and chimeric PCR artifacts through rigorous quality control measures. However, there has been little effort towards understanding the effect of multi-template PCR biases on microbial community structure. In this study, we used three bacterial and three archaeal mock communities consisting of, respectively, 33 bacterial and 24 archaeal 16S rRNA gene sequences combined in different proportions to compare the influences of (1) sequencing depth, (2) sequencing artifacts (sequencing errors and chimeric PCR artifacts), and (3) biases in multi-template PCR, towards the interpretation of community structure in pyrosequencing datasets. We also assessed the influence of each of these three variables on alpha- and beta-diversity metrics that rely on the number of OTUs alone (richness) and those that include both membership and the relative abundance of detected OTUs (diversity). As part of this study, we redesigned bacterial and archaeal primer sets that target the V3-V5 region of the 16S rRNA gene, along with multiplexing barcodes, to permit simultaneous sequencing of PCR products from the two domains. We conclude that the benefits of deeper sequencing efforts extend beyond greater OTU detection and result in higher precision in beta-diversity analyses by reducing the variability between replicate libraries, despite the presence of more sequencing artifacts. Additionally, spurious OTUs resulting from sequencing errors have a significant impact on richness or shared-richness based alpha- and beta-diversity metrics, whereas metrics that utilize community structure (including both richness and relative abundance of OTUs) are minimally affected by spurious OTUs. However, the greatest obstacle towards accurately evaluating community structure are the errors in estimated mean relative abundance of each detected OTU due to biases associated with multi-template PCR reactions.", "link"=>"http://www.mendeley.com/research/pcr-biases-distort-bacterial-archaeal-community-structure-pyrosequencing-datasets", "reader_count"=>386, "reader_count_by_academic_status"=>{"Unspecified"=>11, "Professor > Associate Professor"=>23, "Librarian"=>1, "Researcher"=>90, "Student > Doctoral Student"=>28, "Student > Ph. D. Student"=>124, "Student > Postgraduate"=>13, "Student > Master"=>55, "Other"=>7, "Student > Bachelor"=>17, "Lecturer"=>7, "Lecturer > Senior Lecturer"=>1, "Professor"=>9}, "reader_count_by_user_role"=>{"Unspecified"=>11, "Professor > Associate Professor"=>23, "Librarian"=>1, "Researcher"=>90, "Student > Doctoral Student"=>28, "Student > Ph. D. 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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/311606", "https://ndownloader.figshare.com/files/311711", "https://ndownloader.figshare.com/files/311797", "https://ndownloader.figshare.com/files/311887", "https://ndownloader.figshare.com/files/311952", "https://ndownloader.figshare.com/files/311974", "https://ndownloader.figshare.com/files/312085", "https://ndownloader.figshare.com/files/312150", "https://ndownloader.figshare.com/files/312227", "https://ndownloader.figshare.com/files/312321"], "description"=>"<div><p>As 16S rRNA gene targeted massively parallel sequencing has become a common tool for microbial diversity investigations, numerous advances have been made to minimize the influence of sequencing and chimeric PCR artifacts through rigorous quality control measures. However, there has been little effort towards understanding the effect of multi-template PCR biases on microbial community structure. In this study, we used three bacterial and three archaeal mock communities consisting of, respectively, 33 bacterial and 24 archaeal 16S rRNA gene sequences combined in different proportions to compare the influences of (1) sequencing depth, (2) sequencing artifacts (sequencing errors and chimeric PCR artifacts), and (3) biases in multi-template PCR, towards the interpretation of community structure in pyrosequencing datasets. We also assessed the influence of each of these three variables on α- and β-diversity metrics that rely on the number of OTUs alone (richness) and those that include both membership and the relative abundance of detected OTUs (diversity). As part of this study, we redesigned bacterial and archaeal primer sets that target the V3–V5 region of the 16S rRNA gene, along with multiplexing barcodes, to permit simultaneous sequencing of PCR products from the two domains. We conclude that the benefits of deeper sequencing efforts extend beyond greater OTU detection and result in higher precision in β-diversity analyses by reducing the variability between replicate libraries, despite the presence of more sequencing artifacts. Additionally, spurious OTUs resulting from sequencing errors have a significant impact on richness or shared-richness based α- and β-diversity metrics, whereas metrics that utilize community structure (including both richness and relative abundance of OTUs) are minimally affected by spurious OTUs. However, the greatest obstacle towards accurately evaluating community structure are the errors in estimated mean relative abundance of each detected OTU due to biases associated with multi-template PCR reactions.</p> </div>", "links"=>[], "tags"=>["pcr", "biases", "distort", "bacterial", "archaeal", "pyrosequencing", "datasets"], "article_id"=>121470, "categories"=>["Biological Sciences", "Genetics", "Microbiology", "Evolutionary Biology"], "users"=>["Ameet J. Pinto", "Lutgarde Raskin"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0043093.s001", "https://dx.doi.org/10.1371/journal.pone.0043093.s002", "https://dx.doi.org/10.1371/journal.pone.0043093.s003", "https://dx.doi.org/10.1371/journal.pone.0043093.s004", "https://dx.doi.org/10.1371/journal.pone.0043093.s005", "https://dx.doi.org/10.1371/journal.pone.0043093.s006", "https://dx.doi.org/10.1371/journal.pone.0043093.s007", "https://dx.doi.org/10.1371/journal.pone.0043093.s008", "https://dx.doi.org/10.1371/journal.pone.0043093.s009", "https://dx.doi.org/10.1371/journal.pone.0043093.s010"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/PCR_Biases_Distort_Bacterial_and_Archaeal_Community_Structure_in_Pyrosequencing_Datasets/121470", "title"=>"PCR Biases Distort Bacterial and Archaeal Community Structure in Pyrosequencing Datasets", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2012-08-15 00:24:30"}
  • {"files"=>["https://ndownloader.figshare.com/files/591503"], "description"=>"<p>Error bars in panel A represent variation in GC content between replicates of each community resulting from differences in GC content of barcoded reverse primer. Black bars: bacteria, white bars: archaea. The red dotted line in panel B shows the 95% confidence band for the regression line. Black symbols: bacteria, white symbols: archaea. Diamonds (◊) and upper triangle (Δ): large library, Squares (□) and lower triangle (∇): small library.</p>", "links"=>[], "tags"=>["percent", "gc", "bacterial", "archaeal", "mock", "communities", "resulting", "reads", "attributed", "replicates", "454-sequencing", "sequencing", "amplicon"], "article_id"=>261971, "categories"=>["Biological Sciences", "Genetics", "Microbiology", "Evolutionary Biology"], "users"=>["Ameet J. Pinto", "Lutgarde Raskin"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0043093.g001"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_The_mean_percent_GC_content_of_the_three_bacterial_and_three_archaeal_mock_communities_A_and_the_resulting_reads_attributed_to_mock_community_replicates_in_the_final_454_sequencing_output_expressed_as_percent_reads_in_sequencing_library_versus_the_GC_con/261971", "title"=>"The mean percent GC content of the three bacterial and three archaeal mock communities (A) and the resulting reads attributed to mock community replicates in the final 454-sequencing output expressed as percent reads in sequencing library versus the GC content of the amplicon pool (B).", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-08-15 00:32:51"}
  • {"files"=>["https://ndownloader.figshare.com/files/591643"], "description"=>"<p>Open circles: sub-samples of <i>in-silico</i> mock communities with varying number of sequences, red circles: large library, green circles: small library, solid lines: 95% confidence interval band for the <i>in-silico</i> sub-sampling efforts. A–C: bacteria, D–F: archaea, A/D: mock1, B/E: mock 2, C/F: mock 3. Theoretical taxa detection frequencies for mock community 1 (bacteria and archaea) are 1.0 for most <i>in-silico</i> sub-sampling efforts and hence are not shown in panels A and D.</p>", "links"=>[], "tags"=>["taxa", "detection", "replicate", "mock", "communities", "sequencing", "depths", "compared", "sampling"], "article_id"=>262121, "categories"=>["Biological Sciences", "Genetics", "Microbiology", "Evolutionary Biology"], "users"=>["Ameet J. Pinto", "Lutgarde Raskin"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0043093.g002"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_The_taxa_detection_frequency_for_each_of_the_replicate_mock_communities_at_different_sequencing_depths_are_compared_to_detection_frequency_at_different_theoretical_sampling_depths_/262121", "title"=>"The taxa detection frequency for each of the replicate mock communities at different sequencing depths are compared to detection frequency at different theoretical sampling depths.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-08-15 00:35:21"}
  • {"files"=>["https://ndownloader.figshare.com/files/591790"], "description"=>"<p>A: mock1, B: mock 2, C: mock 3. Dashed line: theoretical relative abundance. The experimental mean relative abundance for small libraries (green circles) and large libraries (red circles) are shown and error bars indicate standard deviations for triplicate samples. The grey box indicates a sequence that was not detected in any community; the black box indicates an OTU that consisted of two sequences at a similarity cutoff of 3%.</p>", "links"=>[], "tags"=>["abundance", "sequences", "bacterial", "mock"], "article_id"=>262289, "categories"=>["Biological Sciences", "Genetics", "Microbiology", "Evolutionary Biology"], "users"=>["Ameet J. Pinto", "Lutgarde Raskin"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0043093.g003"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Relative_abundance_of_sequences_used_to_generate_bacterial_mock_communities_/262289", "title"=>"Relative abundance of sequences used to generate bacterial mock communities.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-08-15 00:38:09"}
  • {"files"=>["https://ndownloader.figshare.com/files/592001"], "description"=>"<p>A: mock1, B: mock 2, C: mock 3. Dashed line: theoretical relative abundance. The experimental mean relative abundance for small libraries (green circles) and large libraries (red circles) are shown and error bars indicate standard deviations for triplicate samples. The black box indicates an OTU that consisted of two sequences at a similarity cutoff of 3%.</p>", "links"=>[], "tags"=>["abundance", "sequences", "archaeal", "mock"], "article_id"=>262496, "categories"=>["Biological Sciences", "Genetics", "Microbiology", "Evolutionary Biology"], "users"=>["Ameet J. Pinto", "Lutgarde Raskin"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0043093.g004"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Relative_abundance_of_sequences_used_to_generate_archaeal_mock_communities_/262496", "title"=>"Relative abundance of sequences used to generate archaeal mock communities.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-08-15 00:41:36"}
  • {"files"=>["https://ndownloader.figshare.com/files/592206"], "description"=>"<p>A–C: bacteria, D–F: archaea. Black lines: theoretical, green lines: small libraries, red lines: large libraries. The Kolmogorov-Smirnov statistics at the left bottom of each panel are for comparisons between large and small libraries. The Kolmogorov-Smirnov statistics to the right of each panel are for comparisons between the large libraries of m1/m2 and m1/m3.</p>", "links"=>[], "tags"=>["abundance", "profiles", "bacterial", "archaeal", "mock"], "article_id"=>262694, "categories"=>["Biological Sciences", "Genetics", "Microbiology", "Evolutionary Biology"], "users"=>["Ameet J. Pinto", "Lutgarde Raskin"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0043093.g005"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Rank_abundance_profiles_for_the_bacterial_and_archaeal_mock_communities_/262694", "title"=>"Rank abundance profiles for the bacterial and archaeal mock communities.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-08-15 00:44:54"}
  • {"files"=>["https://ndownloader.figshare.com/files/592329"], "description"=>"<p>A–D: bacteria, E–H: archaea. Black bars: theoretical, red bars: large libraries, red-hashed bars: large libraries with spurious sequences removed, green bars: small libraries, green-hashed bars: small libraries with spurious sequences removed. The error bars indicate standard deviations for triplicate samples.</p>", "links"=>[], "tags"=>["metrics", "calculated", "bacterial", "archaeal", "mock"], "article_id"=>262820, "categories"=>["Biological Sciences", "Genetics", "Microbiology", "Evolutionary Biology"], "users"=>["Ameet J. Pinto", "Lutgarde Raskin"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0043093.g006"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Diversity_metrics_calculated_for_the_bacterial_and_archaeal_mock_communities_/262820", "title"=>"Diversity metrics calculated for the bacterial and archaeal mock communities.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-08-15 00:47:00"}
  • {"files"=>["https://ndownloader.figshare.com/files/592449"], "description"=>"<p>A–C: bacteria, D–F: archaea. A/D: m1, B/E: m2, C/F: m3. Black squares indicate the theoretical mock community and the small open circles denote the <i>in-silico</i> sequencing efforts at sampling depths varying from 1 to 90%. The red filled squares and red open squares represent the large libraries with and without spurious OTUs, respectively, while green filled triangles and green open triangles indicate the small libraries with and without spurious OTUs, respectively. The blue circle is the centroid of the experimental libraries.</p>", "links"=>[], "tags"=>["axes", "bacterial", "archaeal", "communities", "constructed", "morisita-horn"], "article_id"=>262932, "categories"=>["Biological Sciences", "Genetics", "Microbiology", "Evolutionary Biology"], "users"=>["Ameet J. Pinto", "Lutgarde Raskin"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0043093.g007"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Principal_coordinate_axes_plot_for_bacterial_and_archaeal_communities_constructed_using_the_Morisita_Horn_distance_D_MH_/262932", "title"=>"Principal coordinate axes plot for bacterial and archaeal communities constructed using the Morisita-Horn distance (D<sub>MH</sub>).", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-08-15 00:48:52"}
  • {"files"=>["https://ndownloader.figshare.com/files/592609"], "description"=>"<p>A–C: bacteria, D–F: archaea. A/D: m1–m2, B/E: m1–m3, C/F: m2–m3. Nine pairwise comparisons generated between three replicate libraries for each community were used to construct each box.</p>", "links"=>[], "tags"=>["pairwise", "morisita-horn", "bacterial", "archaeal", "mock", "communities"], "article_id"=>263094, "categories"=>["Biological Sciences", "Genetics", "Microbiology", "Evolutionary Biology"], "users"=>["Ameet J. Pinto", "Lutgarde Raskin"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0043093.g008"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Comparisons_of_pairwise_Morisita_Horn_distance_between_bacterial_and_archaeal_mock_communities_to_the_theoretical_pairwise_distances_/263094", "title"=>"Comparisons of pairwise Morisita-Horn distance between bacterial and archaeal mock communities to the theoretical pairwise distances.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-08-15 00:51:34"}
  • {"files"=>["https://ndownloader.figshare.com/files/592707"], "description"=>"<p>Degeneracy code: R = A/G, Y = C/T, W = A/T, H = A/C/T.</p><p>Phylum and order level coverage for bacteria and archaea are provided in <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0043093#pone.0043093.s001\" target=\"_blank\">Figure S1</a>.</p>", "links"=>[], "tags"=>["archaeal", "primers", "targeting", "sequences", "respective", "rdp"], "article_id"=>263195, "categories"=>["Biological Sciences", "Genetics", "Microbiology", "Evolutionary Biology"], "users"=>["Ameet J. Pinto", "Lutgarde Raskin"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0043093.t001"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Bacterial_and_archaeal_primers_targeting_the_V3_8211_V5_region_of_the_sequences_used_in_this_study_and_their_respective_coverage_for_the_sequences_in_the_RDP_database_release_10_/263195", "title"=>"Bacterial and archaeal primers targeting the V3–V5 region of the sequences used in this study and their respective coverage for the sequences in the RDP database (release 10).", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2012-08-15 00:53:15"}

PMC Usage Stats | Further Information

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Relative Metric

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