Metagenomic sequencing of marine periphyton: taxonomic and functional insights into biofilm communities

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.

Marine biofilms: diversity of communities and of chemical cues

“…Concerning lifestyle, Pepe‐Ranney and Hall () found a difference between biofilm and planktonic bacterial communities, the former showing a higher diversity of alphaproteobacteria. Planktonic species of Chlorophyta and Haptophyta are other widely observed components of biofilm communities (Costas et al ., ), as are planctomycetes, which adhere to different surfaces in aquatic environments such as marine sediments (Nocker et al ., ), diatom cells, seaweeds, macrophytes and artificial surfaces (Sanli et al ., ).…”

Marine Biofilms: A Successful Microbial Strategy With Economic Implications

“…On the other hand, microphytobenthos is used in marine ecosystems to describe the photosynthetic microorganisms, such as cyanobacteria and eukaryotic algae, that adhere to illuminated sediments (MacIntyre et al, 1996). Nevertheless, various definitions of these terms, such as the definition of periphyton communities as complex phototrophic, multispecies biofilms attached to surfaces in aquatic environments, including marine habitats (Sanli et al, 2015), can be found in the literature. For this reason, the broader term "biofilm" will be used throughout this manuscript.…”

Water quality, ecological processes and management procedures in a periphyton biofiltration system in mariculture: A statistical analysis

“…Marine periphyton communities include, in addition to photoautotrophic organisms, also nitrifying bacteria and heterotrophic organisms that metabolize organic matter nitrogen (Sanli et al., ). These populations, and the resulting nitrogen cycling in the periphyton compartment, can be influenced by management (e.g., nitrogen input, water exchange rate, silicate enrichment and cleaning of the water transmission system) and by biological processes developing in the tanks (uptake of inorganic N by algae and nitrifying bacteria, release of inorganic N by decomposing bacteria and other heterotrophic organisms, competition among them all, as well as seasonality).…”