Abstract
Periphyton communities are complex phototrophic, multispecies biofilms that develop on surfaces in aquatic environments. These communities harbor a large diversity of organisms comprising viruses, bacteria, algae, fungi, protozoans, and metazoans. However, thus far the total biodiversity of periphyton has not been described. In this study, we use metagenomics to characterize periphyton communities from the marine environment of the Swedish west coast. Although we found approximately ten times more eukaryotic rRNA marker gene sequences compared to prokaryotic, the whole metagenome-based similarity searches showed that bacteria constitute the most abundant phyla in these biofilms. We show that marine periphyton encompass a range of heterotrophic and phototrophic organisms. Heterotrophic bacteria, including the majority of proteobacterial clades and Bacteroidetes, and eukaryotic macro-invertebrates were found to dominate periphyton. The phototrophic groups comprise Cyanobacteria and the alpha-proteobacterial genus Roseobacter, followed by different micro- and macro-algae. We also assess the metabolic pathways that predispose these communities to an attached lifestyle. Functional indicators of the biofilm form of life in periphyton involve genes coding for enzymes that catalyze the production and degradation of extracellular polymeric substances, mainly in the form of complex sugars such as starch and glycogen-like meshes together with chitin. Genes for 278 different transporter proteins were detected in the metagenome, constituting the most abundant protein complexes. Finally, genes encoding enzymes that participate in anaerobic pathways, such as denitrification and methanogenesis, were detected suggesting the presence of anaerobic or low-oxygen micro-zones within the biofilms.
Highlights
Metagenomics is defined as the culture-independent genomic analysis of an assemblage of microorganisms (Riesenfeld et al, 2004) and has had a profound impact on our understanding of the biosphere (O’Malley and Dupré, 2009; Heidelberg et al, 2010; Tseng and Tang, 2014)
We adopted several strategies for taxonomic and functional annotation, including the similarity searches against the databases of NCBI GenBank nt and nr, SILVA, Swiss-Prot, KEGG Orthology (KO), CAZy, PFAM, and TIGRFAMs, but the percentage of reads of unknown origin – that is, sequences whose taxonomic and functional nature we were unable to deduce through sequence analysis – remained high (78.9%)
The high percentage of sequences of unknown origin indicates that metagenomic sequencing of communities with large proportions of eukaryotes requires even higher sequencing depth
Summary
Metagenomics is defined as the culture-independent genomic analysis of an assemblage of microorganisms (Riesenfeld et al, 2004) and has had a profound impact on our understanding of the biosphere (O’Malley and Dupré, 2009; Heidelberg et al, 2010; Tseng and Tang, 2014). The majority of published metagenomics studies so far has focused either on free-living microbiota such as plankton in the aquatic environment, microbes in air and soil, or host-associated communities living in and on plants and animals. Biofilms are highly structured agglomerations of microorganisms that are attached to surfaces and are ubiquitous in the environment (Costerton et al, 1995). The EPS matrix confers adhesive properties to the biofilm for surface attachment and mechanical stability. It functions as an external compartment for organisms where degradation of xenobiotics and biomolecules (Wuertz et al, 2004), intercellular communication (de Kievit, 2009), horizontal gene transfer (Chia et al, 2008), and various other collaborative and antagonistic interactions take place. The heterogeneity of biofilms and the metabolism of the various biofilm members, results in physicochemical micro-zones with sharp gradients of metabolic substrates and products (Stewart and Franklin, 2008)
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