Deep-Sea Biofilms, Historic Shipwreck Preservation and the Deepwater Horizon Spill

Rachel L Mugge,Melissa L Brock,Jason S Lee,Robert A Church,Melanie Damour,Jennifer L Salerno,Leila J Hamdan

doi:10.3389/fmars.2019.00048

Abstract

Exposure to oil from the Deepwater Horizon spill may have lasting impacts on preservation of historic shipwrecks in the Gulf of Mexico. Submerged steel structures, including shipwrecks, serve as artificial reefs and become hotspots of biodiversity in the deep-sea. Marine biofilms on submerged structures support settlement of micro- and macrobiota and may enhance and protect against corrosion. Disruptions in the local environment, including oil spills, may impact the role that biofilms play in reef preservation. To determine how the Deepwater Horizon spill potentially impacted shipwreck biofilms and the functional roles of the biofilm microbiome, experiments containing carbon steels disks (CSDs) were placed at five historic shipwreck sites located within, and external to the benthic footprint of the Deepwater Horizon spill. The CSDs were incubated for 16 weeks to enable colonization by biofilm-forming microorganisms and to provide time for in situ corrosion to occur. Biofilms from the CSDs, as well as sediment and water microbiomes, were collected and analyzed by 16S rRNA amplicon gene sequencing to describe community composition and determine the source of taxa colonizing biofilms. Biofilm metagenomes were sequenced to compare differential gene abundances at spill-impacted and reference sites. Biofilms were dominated by Zeta-, Alpha-, Epsilon and Gammaproteobacteria. Sequences affiliated with the Mariprofundus and Sulfurimonas genera were prolific, and Roseobacter, and Colwellia genera were also abundant. Analysis of 16S rRNA sequences from sediment, water, and biofilms revealed sediment to be the main known source of taxa to biofilms at impacted sites. Differential gene abundance analysis revealed the two-component response regulator CreC, a gene involved in environmental stress response, to be elevated at reference sites compared to impacted sites within the spill plume fallout area on the seafloor. Genes for chemotaxis, motility, and alcohol dehydrogenases were differentially abundant at reference vs. impacted sites. Metal loss on CSDs was elevated at sites within the spill fallout plume. Time series images reveal that metal loss at a heavily impacted site, the German Submarine U-166, has accelerated since the spill in 2010. This study provides evidence that spill residues on the seafloor may impact biofilm communities and the preservation of historic steel shipwrecks.

Highlights

Biofilms form on surfaces in the marine environment when microorganisms adhere to solid substrates and develop a thin layer of cells and extracellular polymeric substances (EPS) (Qian et al, 2007)
Archaeal sequences in sediment were more abundant than bacteria; bacterial diversity and operational taxonomic units (OTUs) richness exceeded archaeal metrics at all sites
The Proteobacteria were highly abundant in surface sediments at all sites, and Delta, Gamma, and Alpha-proteobacteria accounted for over 50% of sequences (Supplementary Figure S1)

Summary

Introduction

Biofilms form on surfaces in the marine environment when microorganisms adhere to solid substrates and develop a thin layer of cells and extracellular polymeric substances (EPS) (Qian et al, 2007). EPS provide stability, protection, nutrition, and recruitment cues to the microbiome, and promote the recruitment of macro-organisms on artificial reefs (Svane and Petersen, 2001). Spatial organization, and interspecies interaction are determined by physical, biological, and chemical factors in the local environment (Garrett et al, 2008; Brauer et al, 2015). The dominant phylotypes in a biofilm are dictated by environmental conditions and the substrate to which they attach. Historic shipwrecks provide substrate for attachment of marine biofilms. Fauna recruit to the shipwreck’s surface, creating an artificial reef that becomes a diverse community of organisms. Marine biofilm maturation in shallow water (less than 200 m) may occur rapidly (4–30 days) (Teitzel and Parsek, 2003; Acuña et al, 2006; Barraud et al, 2006; Bermont-Bouis et al, 2007; Nithya et al, 2010), little is known about the formation of marine biofilms in the deep sea (McBeth and Emerson, 2016)

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