Metagenomic Analysis of Zinc Surface–Associated Marine Biofilms
Biofilms are a significant source of marine biofouling. Marine biofilm communities are established when microorganisms adhere to immersed surfaces. Despite the microbe-inhibiting effect of zinc surfaces, microbes can still attach to the surface and form biofilms. However, the diversity of biofilm-forming microbes that can attach to zinc surfaces and their common functional features remain elusive. Here, by analyzing 9,000,000 16S rRNA gene amplicon sequences and 270 Gb of metagenomic data, we comprehensively explored the taxa and functions related to biofilm formation in subtidal zones of the Red Sea. A clear difference was observed between the biofilm and adjacent seawater microbial communities in terms of the taxonomic structure at phylum and genus levels, and a huge number of genera were only present in the biofilms. Saturated alpha-diversity curves suggested the existence of more than 14,000 operational taxonomic units in one biofilm sample, which is much higher than previous estimates. Remarkably, the biofilms contained abundant and diverse transposase genes, which were localized along microbial chromosomal segments and co-existed with genes related to metal ion transport and resistance. Genomic analyses of two cyanobacterial strains that were abundant in the biofilms revealed a variety of metal ion transporters and transposases. Our analyses revealed the high diversity of biofilm-forming microbes that can attach to zinc surfaces and the ubiquitous role of transposase genes in microbial adaptation to toxic metal surfaces.
KeywordsMarine biofilm Zinc panel Transposase Metagenome
This study was supported by a research grant from China Ocean Mineral Resource Research and Development Association (COMRRDA17/Sc01) and an award from the King Abdullah University of Science and Technology to P.Y. Qian. The authors are grateful to Ms. Alice Cheung for English editing.
Compliance with Ethical Standards
Conflict of Interest
The authors declare that they have no conflict of interest.
- 12.Lesaulnier CC, Herbold CW, Pelikan C, Berry D, Gérard C, Le Coz X, Gagnot S, Niggemann J, Dittmar T, Singer GA, Loy A (2017) Bottled aqua incognita: microbiota assembly and dissolved organic matter diversity in natural mineral waters. Microbiome 5:126. https://doi.org/10.1186/s40168-017-0344-9 CrossRefGoogle Scholar
- 19.Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Peña AG, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Turnbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336. https://doi.org/10.1038/nmeth.f.303 CrossRefGoogle Scholar
- 22.Hammer Ř, Harper DAT, Ryan PD (2001) PAST: paleontological statistics software package for education and data analysis. Palaeontol Electron 4:9Google Scholar
- 29.Zhang W, Wang Y, Bougouffa S, Tian R, Cao H, Li Y, Cai L, Wong YH, Zhang G, Zhou G, Zhang X, Bajic VB, Al-Suwailem A, Qian PY (2015) Synchronized dynamics of bacterial niche-specific functions during biofilm development in a cold seep brine pool. Environ Microbiol 7:4089–4104. https://doi.org/10.1111/1462-2920.12978 CrossRefGoogle Scholar
- 32.Parks DH, Imelfort M, Skennerton CT, Hugenholtz P, Tyson GW (2015) CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes. Genome Res gr-186072. https://doi.org/10.1101/gr.186072.114
- 37.Lee OO, Chung HC, Yang J, Wang Y, Dash S, Wang H, Qian PY (2014) Molecular techniques revealed highly diverse microbial communities in natural marine biofilms on polystyrene dishes for invertebrate larval settlement. Microb Ecol 68:81–93. https://doi.org/10.1007/s00248-013-0348-3 CrossRefGoogle Scholar
- 40.Tetaz TJ, Luke RKJ (1983) Plasmid-controlled resistance to copper in Escherichia coli. J Bacteriol 154:1263–1268Google Scholar
- 41.Gupta A, Maynes M, Silver S (1998) Effects of halides on plasmid-mediated silver resistance in Escherichia coli. Appl Environ Microbiol 64:5042–5045Google Scholar
- 49.Bullerjahn GS, Post AF (2014) Physiology and molecular biology of aquatic cyanobacteria. Front Microbiol 5(359). https://doi.org/10.3389/fmicb.2014.00359
- 50.Pessi IS, Pushkareva E, Lara Y, Borderie F, Wilmotte A, Elster J (2018) Marked succession of cyanobacterial communities following glacier retreat in the high Arctic. Microb Ecol:1–12. https://doi.org/10.1007/s00248-018-1203-3