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Biofilms Constitute a Bank of Hidden Microbial Diversity and Functional Potential

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Biofilms Constitute a Bank of Hidden Microbial Diversity and Functional Potential Marine biofilms constitute a bank of hidden microbial diversity and functional potential Item Type Article Authors Zhang, Weipeng; Ding, Wei; Li, Yong-Xin; Tam, Chunkit; Bougouffa, Salim; Wang, Ruojun; Pei, Bite; Chiang, Hoyin; Leung, Pokman; Lu, Yanhong; Sun, Jin; Fu, He; Bajic, Vladimir B.; Liu, Hongbin; Webster, Nicole S.; Qian, Pei-Yuan Citation Zhang W, Ding W, Li Y-X, Tam C, Bougouffa S, et al. (2019) Marine biofilms constitute a bank of hidden microbial diversity and functional potential. Nature Communications 10. Available: http:// dx.doi.org/10.1038/s41467-019-08463-z. Eprint version Publisher's Version/PDF DOI 10.1038/s41467-019-08463-z Publisher Springer Nature Journal Nature Communications Rights This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/ by/4.0/. Download date 28/09/2021 05:24:48 Item License http://creativecommons.org/licenses/by/4.0/ Link to Item http://hdl.handle.net/10754/631009 Biofilms constitute a bank of hidden microbial diversity and functional potential in the oceans Zhang et al Supplementary Information 1 1 3 . 5 6 4 . 8 2 7 Pacific Ocean Indian Ocean Atlantic Ocean Pacific Ocean Biofilm and seawater in current study Tara seawater Supplementary Figure 1. Geographic distribution of the eight sampling locations of the 101 biofilms. (1) South Atlantic, (2) Red Sea, (3) Hong Kong Water, (4) Yung Shu O Bay, (5) East China Sea, (6) South China Sea 1, (7) South China Sea 2, and (8) South China Sea 3. The majority of biofilms were developed on Petri dishes and man- made panels immersed in the subtidal zone. Biofilms were sampled from Hong Kong seawater in different months during 2013-2017. During biofilm development, 24 adjacent seawater samples were collected from the locations (2), (3), (4), and (6) for comparison. Sampling locations of the 67 Tara seawater samples (surface seawater metagenomes downloaded for comparison with the biofilms) are also shown. 2 a c 9 cm 5 cm Al PEEK PVC b PTFE SS Ti e d 11 cm 25 cm Supplementary Figure 2. Devices and materials used for biofilm development and collection. Biofilms were developed on a) Petri dishes, b) zinc panels with antifoulant, c, d) small panels of man-made materials fixed in a container with matching slots, and e, naturally-occurring rocks. Abbreviations: aluminum (Al), poly(ether-ether-ketone) (PEEK), polytetrafluoroethylene (PTFE), poly(vinyl chloride) (PVC), stainless steel (SS) and titanium (Ti). 3 a b c 1 2 3 4 5 6 Supplementary Figure 3. Microscopic observation of biofilms under a confocal laser scanning microscope. a) Overall two-dimensional structure. Scale bar: 10μm.b) Overall three-dimensional structure. Scale bar: 100μm.c) Six dissected layers, from the top to the bottom of the biofilm. Scale bar: 25μm. 4 27000 24000 21000 18000 15000 12000 Observed OTUs Observed 9000 6000 3000 0 1 20 40 60 80 101 Number of biofilm samples Supplementary Figure 4. Accumulation curve of detected OTUs for 100-fold permuted sampling of the biofilms. Minimal increases towards the end of sampling were observed. Calculations were performed using the ‘vegan’ package in R with 100 permutations. In a boxplot, central line represents the median, bounds represent upper and lower quartiles, and whiskers represent maximum and minimum. 5 a 2492 3520 5101 6944 Biofilm ± ± ± ± 279 28 26 1 637 1122 2008 3434 ± ± ± ± 68 2 5 0 Seawater 2348 3166 3937 4700 ± ± ± ± 68 3 5 1 20 40 80 160 million Reads number 0.6 b Biofilm Seawater 0.5 0.4 0.3 0.2 Specific OTU SpecificOTU Ratio 0.1 0 20 40 80 160 million Reads number Supplementary Figure 5. Correlation between biofilm or seawater specificity and sequencing depth. A series of numbers (20, 40, 80, and 160 million) of reads were randomly extracted, from one deeply sequenced biofilm metagenome and one seawater metagenome. a) The number of OTUs specific to biofilms or seawater. b) The ratio of specific OTUs in biofilms or seawater compared to the total number of OTUs in biofilms and seawater. Dot lines indicate the change of the specific OTU ratios along with the increase of sequencing depth. Errors represent standard deviations. 6 Biofilm New seawater Tara seawater 100% 90% 80% 70% 60% 50% 40% Relativeabundance 30% 20% 10% 0% Alphaproteobacteria Betaproteobacteria Gammaproteobacteria Deltaproteobacteria Epsilonproteobacteria Zetaproteobacteria Acidobacteria Actinobacteria Aquificae Bacteroidetes Chlamydiae Chlorobi Chloroflexi Chrysiogenetes Crenarchaeota Cyanobacteria Deferribacteres Deinococcus-Thermus Dictyoglomi Elusimicrobia Euryarchaeota Fibrobacteres Firmicutes Fusobacteria Gemmatimonadetes Korarchaeota Lentisphaerae Nanoarchaeota Nitrospirae Planctomycetes Spirochaetes Synergistetes Tenericutes Thaumarchaeota Thermodesulfobacteria Thermotogae Verrucomicrobia Unclassified Supplementary Figure 6. Taxonomic composition based on protein-coding marker genes derived from metagenomes. The figure shows the distribution of all phyla across the 101 biofilm and 24 seawater metagenomes that were sequenced as part of the current study and the 67 previously published Tara Oceans metagenomes. The order of samples in this figure is the same as that in Supplementary Data 1. mOTU 7 Biofilm New seawater Tara seawater 100% 90% 80% 70% 60% 50% 40% Relativeabundance 30% 20% 10% 0% Alphaproteobacteria Betaproteobacteria Gammaproteobacteria Deltaproteobacteria Epsilonproteobacteria Zetaproteobacteria Acidobacteria Actinobacteria Bacteroidetes Caldithrix Chlamydiae Chloroflexi Crenarchaeota Cyanobacteria Deinococcus_Thermus Euryarchaeota Firmicutes Gemmatimonadetes GN02 Lentisphaerae Nitrospirae Parvarchaeota Planctomycetes SAR406 SBR1093 Spirochaetes Tenericutes Verrucomicrobia Minor or unclassified Supplementary Figure 7. Taxonomic composition based on analysis of 16S miTags following gene length and copy number normalization. Abundant phyla (the top 30 phyla in terms of maximum relative abundance) are shown with all other phyla grouped together as ‘Minor’. The order of samples in this figure is the same as that in Supplementary Data 1. 8 20% Biofilm-16S miTags *** 18% Biofilm-16S miTags with normalization *** Biofilm-Protein-coding maker gene 16% Seawater-16S miTags *** 14% Seawater-16S miTags with normalization 12% Seawater-Protein-coding maker gene 10% *** *** 8% Relative abundance Relative *** *** *** 6% *** 4% 2% *** *** *** 0 Acidobacteria Chloroflexi Deltaproteobacteria Planctomycetes Supplementary Figure 8. Representative microbial phyla differentially enriched in the biofilms (101 biofilms compared with 91 seawater samples). Abundance was calculated by analyzing 16S miTags, 16S miTags normalized by copy number and gene length, and protein-coding marker genes. *** p-value <0.001 (Mann-Whitney U test). In a boxplot, central line represents the median, bounds represent upper and lower quartiles, and whiskers represent maximum and minimum. 9 0.5 0.4 0.3 0.2 (10.7%) 0.1 2 PCoA 0.0 -0.1 -0.2 -0.3 -0.3 -0.2 -0.1 0.0 0.1 0.2 0.3 0.4 PCoA 1 (34.2%) Supplementary Figure 9. Similarity of the microbial communities based on 16S miTags without data size normalization. Jaccard distances were calculated based on an OTU matrix derived from 16S miTags without data size normalization, and visualized through PCoA. The blue dots represent biofilms while the red dots represent seawater microbial communities. 10 0.40 0.35 0.30 0.25 Natural rock 0.20 0.15 0.10 2 (11.6%) 2 0.05 Co P 0.00 Artificial panel -0.05 -0.10 Seawater -0.15 -0.20 -0.25 -0.24 -0.16 -0.08 0.00 0.08 0.16 0.24 0.32 0.40 0.48 PCo 1 (20.1%) Supplementary Figure 10. Similarity of the biofilms developed on artificial panels and natural rocks, as well as seawater microbial communities. All samples included for this analysis were collected in Hong Kong water in 2017. Jaccard similarity derived from the OTU matrix was illustrated by PCoA. These analyses were performed after normalizing the different 16S miTag data to the same library size, i.e. 10,000 sequences per sample. 11 100% 90% Biofilm-specific protein-coding genes 80% 70% 60% 50% 40% Relative abundance abundance Relative 30% 20% Common protein-coding genes 10% 0% 101 biofilms Biofilm-specific Remove Select genes present BSGC BCGC protein-coding genes redundant genes in >99 biofilms Supplementary Figure 11. Distribution of biofilm-specific protein-coding genes in the 101 biofilm metagenomes. Biofilm-specific protein-coding genes (redundant genes without CD-HIT process) were identified by searching against the OM-RGC and the seawater data from the current study. ‘Common protein-coding genes’ are genes shared by both biofilm and seawater metagenomes. Biofilm-specific protein-coding genes were subsequently combined and subjected to CD-HIT to generate a nonredundant biofilm-specific gene catalogue (BSGC). The BSGC genes present in more than 99 biofilms are defined as the biofilm
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