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Marine biofilms constitute a bank of hidden microbial diversity and functional potential.

ABSTRACT: Recent big data analyses have illuminated marine microbial diversity from a global perspective, focusing on planktonic microorganisms. Here, we analyze 2.5 terabases of newly sequenced datasets and the Tara Oceans metagenomes to study the diversity of biofilm-forming marine microorganisms. We identify more than 7,300 biofilm-forming 'species' that are undetected in seawater analyses, increasing the known microbial diversity in the oceans by more than 20%, and provide evidence for differentiation across oceanic niches. Generation of a gene distribution profile reveals a functional core across the biofilms, comprised of genes from a variety of microbial phyla that may play roles in stress responses and microbe-microbe interactions. Analysis of 479 genomes reconstructed from the biofilm metagenomes reveals novel biosynthetic gene clusters and CRISPR-Cas systems. Our data highlight the previously underestimated ocean microbial diversity, and allow mining novel microbial lineages and gene resources.

SUBMITTER: Zhang W

PROVIDER: S-EPMC6355793 | biostudies-literature | 2019 Jan

REPOSITORIES: biostudies-literature

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Marine biofilms constitute a bank of hidden microbial diversity and functional potential.

Zhang Weipeng W Ding Wei W Li Yong-Xin YX Tam Chunkit C Bougouffa Salim S Wang Ruojun R Pei Bite B Chiang Hoyin H Leung Pokman P Lu Yanhong Y Sun Jin J Fu He H Bajic Vladimir B VB Liu Hongbin H Webster Nicole S NS Qian Pei-Yuan PY

Nature communications 20190131 1

Recent big data analyses have illuminated marine microbial diversity from a global perspective, focusing on planktonic microorganisms. Here, we analyze 2.5 terabases of newly sequenced datasets and the Tara Oceans metagenomes to study the diversity of biofilm-forming marine microorganisms. We identify more than 7,300 biofilm-forming 'species' that are undetected in seawater analyses, increasing the known microbial diversity in the oceans by more than 20%, and provide evidence for differentiation ...[more]

PMID: 30705275

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Project description:Marine biofilms are essential biological components that transform built structures into artificial reefs. Anthropogenic contaminants released into the marine environment, such as crude oil and chemical dispersant from an oil spill, may disrupt the diversity and function of these foundational biofilms. To investigate the response of marine biofilm microbiomes from distinct environments to contaminants and to address microbial functional response, biofilm metagenomes were analyzed from two short-term microcosms, one using surface seawater (SSW) and the other using deep seawater (DSW). Following exposure to crude oil, chemical dispersant, and dispersed oil, taxonomically distinct communities were observed between microcosms from different source water challenged with the same contaminants and higher Shannon diversity was observed in SSW metagenomes. Marinobacter, Colwellia, Marinomonas, and Pseudoalteromonas phylotypes contributed to driving community differences between SSW and DSW. SSW metagenomes were dominated by Rhodobacteraceae, known biofilm-formers, and DSW metagenomes had the highest abundance of Marinobacter, associated with hydrocarbon degradation and biofilm formation. Association of source water metadata with treatment groups revealed that control biofilms (no contaminant) harbor the highest percentage of significant KEGG orthologs (KOs). While 70% functional similarity was observed among all metagenomes from both experiments, functional differences between SSW and DSW metagenomes were driven primarily by membrane transport KOs, while functional similarities were attributed to translation and signaling and cellular process KOs. Oil and dispersant metagenomes were 90% similar to each other in their respective experiments, which provides evidence of functional redundancy in these microbiomes. When interrogating microbial functional redundancy, it is crucial to consider how composition and function evolve in tandem when assessing functional responses to changing environmental conditions within marine biofilms. This study may have implications for future oil spill mitigation strategies at the surface and at depth and also provides information about the microbiome functional responses of biofilms on steel structures in the marine built environment.

Project description:Creating and maintaining an appropriate chemical environment is essential for biomineralization, the process by which organisms precipitate minerals to form their shells or skeletons, yet the mechanisms involved in maintaining calcifying fluid chemistry are not fully defined. In particular, the role of microorganisms in facilitating or hindering animal biomineralization is poorly understood. Here, we investigated the taxonomic diversity and functional potential of microbial communities inhabiting oyster calcifying fluid. We used shotgun metagenomics to survey calcifying fluid microbial communities from three different oyster harvesting sites. There was a striking consistency in taxonomic composition across the three collection sites. We also observed archaea and viruses that had not been previously identified in oyster calcifying fluid. Furthermore, we identified microbial energy-conserving metabolisms that could influence the host's calcification, including genes involved in sulfate reduction and denitrification that are thought to play pivotal roles in inorganic carbon chemistry and calcification in microbial biofilms. These findings provide new insights into the taxonomy and functional capacity of oyster calcifying fluid microbiomes, highlighting their potential contributions to shell biomineralization, and contribute to a deeper understanding of the interplay between microbial ecology and biogeochemistry that could potentially bolster oyster calcification.ImportancePrevious research has underscored the influence of microbial metabolisms in carbonate deposition throughout the geological record. Despite the ecological importance of microbes to animals and inorganic carbon transformations, there have been limited studies characterizing the potential role of microbiomes in calcification by animals such as bivalves. Here, we use metagenomics to investigate the taxonomic diversity and functional potential of microbial communities in calcifying fluids from oysters collected at three different locations. We show a diverse microbial community that includes bacteria, archaea, and viruses, and we discuss their functional potential to influence calcifying fluid chemistry via reactions like sulfate reduction and denitrification. We also report the presence of carbonic anhydrase and urease, both of which are critical in microbial biofilm calcification. Our findings have broader implications in understanding what regulates calcifying fluid chemistry and consequentially the resilience of calcifying organisms to 21st century acidifying oceans.

Dataset Information

Marine biofilms constitute a bank of hidden microbial diversity and functional potential.

Publications

Marine biofilms constitute a bank of hidden microbial diversity and functional potential.

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