Michael Cunliffe

Early microbial biofilm formation on marine plastic debris.

An important aspect of the global problem of plastic debris pollution is plastic buoyancy. There is some evidence that buoyancy is influenced by attached biofilms but as yet this is poorly understood. We submerged polyethylene plastic in seawater and sampled weekly for 3 weeks in order to study early stage processes. Microbial biofilms developed rapidly on the plastic and coincided with significant changes in the physicochemical properties of the plastic. Submerged plastic became less hydrophobic and more neutrally buoyant during the experiment. Bacteria readily colonised the plastic but there was no indication that plastic-degrading microorganisms were present. This study contributes to improved understanding of the fate of plastic debris in the marine environment.

The future of the northeast Atlantic benthic flora in a high CO2 world

Seaweed and seagrass communities in the northeast Atlantic have been profoundly impacted by humans, and the rate of change is accelerating rapidly due to runaway CO2 emissions and mounting pressures on coastlines associated with human population growth and increased consumption of finite resources. Here, we predict how rapid warming and acidification are likely to affect benthic flora and coastal ecosystems of the northeast Atlantic in this century, based on global evidence from the literature as interpreted by the collective knowledge of the authorship. We predict that warming will kill off kelp forests in the south and that ocean acidification will remove maerl habitat in the north. Seagrasses will proliferate, and associated epiphytes switch from calcified algae to diatoms and filamentous species. Invasive species will thrive in niches liberated by loss of native species and spread via exponential development of artificial marine structures. Combined impacts of seawater warming, ocean acidification, and increased storminess may replace structurally diverse seaweed canopies, with associated calcified and noncalcified flora, with simple habitats dominated by noncalcified, turf-forming seaweeds.

Microbiology of aquatic surface microlayers

Aquatic surface microlayers are unique microbial ecosystems found at the air-water interface of all open water bodies and are often referred to as the neuston. Unambiguous interpretation of the microbiology of aquatic surface microlayers relies on robust sampling, for which several methods are available. All have particular advantages and disadvantages that make them more or less suited to this task. A key feature of surface microlayers is their role in regulating air-water gas exchange, which affords them a central role in global biogeochemistry that is only now being fully appreciated. The microbial populations in surface microlayers can impact air-water gas exchange through specific biogeochemical processes mediated by particular microbial groups such as methanotrophs or through more general metabolic activity such as the balance of primary production vs. heterotrophy. There have been relatively few studies of surface microlayers that have utilized molecular ecology techniques. The emerging consensus view is that aquatic surface microlayers are aggregate-enriched biofilm environments containing complex microbial communities that are ecologically distinct from those present in the subsurface water immediately below. Future research should focus on unravelling the complex interactions between microbial diversity and the ecosystem function of surface microlayers in order to better understand the important but complex role of microorganisms in Earth system processes.

The sea-surface microlayer is a gelatinous biofilm

One of John McN Sieburth’s many contributions to biological oceanography was his proposal of a hydrated gelatinous surface microlayer film at the air–sea interface (Sieburth, 1983). The purpose of this commentary is to highlight John Sieburth’s contribution to surface ocean science and the recent evidence that supports his proposal of a gelatinous microlayer film. His hypothesis was based on many observations made over several years, including those during a Trichodesmium bloom in the Sargasso Sea, when a distinct slick was reported directly above the bloom (Sieburth and Conover, 1965). At the air–sea interface, the sea-surface microlayer is the physical boundary between the ocean and the atmosphere. Roughly considered to be the uppermost 1 mm of the ocean, the sea-surface microlayer is physico-chemically distinct compared with subsurface water and is characteristically enriched with biogenic organic compounds, such as lipids, proteins and polysaccharides (Liss and Duce, 2005). The presence of the surface film and surface tension properties means the sea-surface microlayer is a unique habitat that is often referred to as the neuston. Bacterial communities that are present in the surface microlayer are known as the bacterioneuston (Liss and Duce, 2005). Surface films occur on all water bodies, marine, estuarine and freshwater, sometimes as visible slicks, and are rapidly reformed after mixing by wind or waves (RC UpstillGoddard, personal communication). The widely known effect of pouring oil on troubled waters occurs naturally, with organic films changing the physical properties of surface water, reducing roughness and affecting air–sea gas transfer (Liss and Duce, 2005). The structure of the sea-surface microlayer film, potentially 70% of the Earth’s surface, is of great importance in the exchange of chemicals between the oceans and the atmosphere. During summer blooms of filamentous cyanobacteria, the net oxygen flux is significantly highly between the atmosphere and the surface microlayer compared with the ocean and the surface microlayer, which highlights the importance of autotrophic and heterotrophic organisms in this environment (Ploug, 2008). Also, bacterial activity within the microlayer can mediate the air–sea flux of other gases, such as methane (Upstill-Goddard et al., 2003). Recent work by Wurl and Holmes (2008) has shed new insights into Sieburth’s proposal, with important implications for marine microbial ecology and oceanography. Sea-surface microlayer and subsurface water samples (1-m depth) were collected from around Singapore and subsequently, the concentrations of transparent exopolymer particles (TEPs) were determined (Wurl and Holmes, 2008). They showed an enrichment of TEPs in the sea-surface microlayer. TEPs are generally formed in surface waters from the coagulation of biogenic polysaccharides (Figure 1), particularly those produced by phytoplankton, and are some of the most ubiquitous gel particles in the marine environment (Verdugo et al., 2004). They are critical in the formation of marine aggregates, acting as the binding matrix or ‘glue’ that holds the aggregate together (Verdugo et al., 2004). An abundance of TEPs in the seasurface microlayer supports Sieburth’s proposal made in 1983. The molecular microbial ecology of the seasurface microlayer has only recently been studied. Franklin et al. (2005) showed that the bacterioneuston at a site in the North Sea was distinctly different compared with subsurface water just 0.4 m below the surface. The bacterioneuston was dominated by two genera, Vibrio and Pseudoalteromonas. Both organisms have physiological characteristics that are indicative of adaptations for biofilm survival (Franklin et al., 2005). If the seasurface microlayer is a gelatinous film, then organisms that have biofilm capabilities will have a selective advantage. More recent evidence published in The ISME Journal supports the observations made in the North Sea by Franklin et al. (2005) and shows distinct bacterioneuston communities are also present in estuarine surface microlayers (Cunliffe et al., 2008). Denaturing gradient gel electrophoresis comparison of bacterial and archaeal 16S rRNA genes from surface microlayer and subsurface water samples at The ISME Journal (2009) 3, 1001–1003 & 2009 International Society for Microbial Ecology All rights reserved 1751-7362/09

Community-level response of coastal microbial biofilms to ocean acidification in a natural carbon dioxide vent ecosystem

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Phylogenetic and functional gene analysis of the bacterial and archaeal communities associated with the surface microlayer of an estuary.

The impacts of ocean acidification on coastal biofilms are poorly understood. Carbon dioxide vent areas provide an opportunity to make predictions about the impacts of ocean acidification. We compared biofilms that colonised glass slides in areas exposed to ambient and elevated levels of pCO(2) along a coastal pH gradient, with biofilms grown at ambient and reduced light levels. Biofilm production was highest under ambient light levels, but under both light regimes biofilm production was enhanced in seawater with high pCO(2). Uronic acids are a component of biofilms and increased significantly with high pCO(2). Bacteria and Eukarya denaturing gradient gel electrophoresis profile analysis showed clear differences in the structures of ambient and reduced light biofilm communities, and biofilms grown at high pCO(2) compared with ambient conditions. This study characterises biofilm response to natural seabed CO(2) seeps and provides a baseline understanding of how coastal ecosystems may respond to increased pCO(2) levels.

Seasonal microbial community dynamics correlate with phytoplankton-derived polysaccharides in surface coastal waters

The surface microlayer (SML) is the thin biogenic film found at the surface of a water body. The SML is poorly understood but has been shown to be important in biogeochemical cycling and sea–air gas exchange. We sampled the SML of the Blyth estuary at two sites (salinities 21 and 31 psu) using 47 mm polycarbonate membranes. DNA was extracted from the SML and corresponding subsurface water (0.4 m depth) and microbial (bacteria and archaea) community analysis was performed using denaturing gradient gel electrophoresis of 16S rRNA gene PCR amplicons. The diversity of bacterial functional genes that encode enzyme subunits for methane monooxygenase (pmoA and mmoX) and carbon monoxide dehydrogenase (coxL) was assessed using PCR, clone library construction and restriction fragment length polymorphism (RFLP) analysis. Methanotroph genes were present only in low copy numbers and pmoA was detected only in subsurface samples. Diversity of mmoX genes was low and most of the clone sequences detected were similar to those of mmoX from Methylomonas spp. Interestingly, some sequences detected in the SML were different from those detected in the subsurface. RFLP analysis of coxL clone libraries indicated a high diversity of carbon monoxide (CO)-utilizing bacteria in the estuary. The habitats of the closely related coxL sequences suggest that CO-utilizing bacteria in the estuary are recruited from both marine and freshwater/terrestrial inputs. In contrast, methanotroph recruitment appears to occur solely from freshwater input into the estuary.

Correlating carbon monoxide oxidation with cox genes in the abundant Marine Roseobacter Clade.

Phytoplankton produce large amounts of polysaccharide gel material known as transparent exopolymer particles (TEP). We investigated the potential links between phytoplankton-derived TEP and microbial community structure in the sea surface microlayer and underlying water at the English Channel time-series station L4 during a spring diatom bloom, and in two adjacent estuaries. Major changes in bacterioneuston and bacterioplankton community structure occurred after the peak of the spring bloom at L4, and coincided with the significant decline of microlayer and water column TEP. Increased abundance of Flavobacteriales and Rhodobacterales in bacterioneuston and bacterioplankton communities at L4 was significantly related to the TEP decline, indicating that both taxa could be responsible. The results suggest that TEP is an important factor in determining microbial diversity in coastal waters, and that TEP utilisation could be a niche occupied by Flavobacteriales and Rhodobacterales.

Complete Genome Sequence of the Aerobic Marine Methanotroph Methylomonas methanica MC09

The Marine Roseobacter Clade (MRC) is a numerically and biogeochemically significant component of the bacterioplankton. Annotation of multiple MRC genomes has revealed that an abundance of carbon monoxide dehydrogenase (CODH) cox genes are present, subsequently implying a role for the MRC in marine CO cycling. The cox genes fall into two distinct forms based on sequence analysis of the coxL gene; forms I and II. The two forms are unevenly distributed across the MRC genomes. Most (18/29) of the MRC genomes contain only the putative form II coxL gene. Only 10 of the 29 MRC genomes analysed have both the putative form II and the definitive form I coxL. None have only the form I coxL. Genes previously shown to be required for post-translational maturation of the form I CODH enzyme are absent from the MRC genomes containing only form II. Subsequent analyses of a subset of nine MRC strains revealed that only MRC strains with both coxL forms are able to oxidise CO.

Dissolved organic carbon and bacterial populations in the gelatinous surface microlayer of a Norwegian fjord mesocosm

Methylomonas methanica MC09 is a mesophilic, halotolerant, aerobic, methanotrophic member of the Gammaproteobacteria, isolated from coastal seawater. Here we present the complete genome sequence of this strain, the first available from an aerobic marine methanotroph.