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August 12, 2010

Biofilms Over Troubled Waters

by Mark O. Martin


The old saying “pouring oil on troubled waters” is a metaphor for bringing peace to a turbulent situation. Recent events in the Gulf of Mexico have proved the contrary, that oil poured (or spilled) upon seawater can produce the very antithesis of calm. After many weeks of concern, and with the long term threat of possible subsurface oil still strong, recent reports note that the oil slicks at the surface have become more difficult to find. What is happening? To be sure, dispersal over time is inevitable, but there may be more to the “vanishing” oil slicks.

What we perceive as the leakage of a toxic fuel into the ocean might be seen as an aliphatic feast by marine microbes. Quite a bit of literature describes the relationship that microbes have with oil (for a review, click here) and the possible role for such microbes in bioremediation of oil spills.


Burning off slicks. Source.

Researchers who investigated the aftermath of prior oil spills found that microbes can be involved in the amelioration of such accidents, acting as natural bioremediation agents, as we'd expect on Planet Microbe. Alkane-degrading microbes can in fact increase in population in response to petroleum contamination, as observed in studies ranging from Antarctica to Spain. However, such studies tend to focus on the impact of oil on shorelines instead of on the ocean surface itself. As I watched televised coverage of the spreading oil slicks in the Gulf, I recalled a short paper I had assigned to my latest microbiology class, which suggested that the very surface of the ocean itself could be thought of as an enormous, but very thin, biofilm. This short review by Cunliffe and Murrell credits the biological oceanographer John McN Sieburth with visualizing the air-sea interface as a gelatinous microlayer—a huge biofilm that may cover 70% of the Earth’s surface! (Click here to listen to an interview with Michael Cunliffe.)

Fig 4

A diagrammatic representation of the neuston including the bacterio-
neuston and TEP. Source.

The upper millimeter of the ocean with its inhabitants is referred to as the neuston, its clearly distinctive microbial communities as the bacterioneuston. These communities reflect the specific environmental and nutritional conditions to be found in that microlayer in marine, estuarine, or fresh water environments. Transparent exopolymer particles (TEPs) synthesized by primary producers form the “lattice” that appears to hold the bacterioneuston in place (see figure). TEPs can act as a food source as well as surfaces for microbial colonization, as they float upward and merge with the presumed surface biofilm.

One study found that the bacterioneuston, in contrast to the microbiota found half a meter below the surface, is dominated by two genera: Vibrio and Pseudoalteromonas. Both appear to be well adapted to life in a biofilm at a liquid-solid interface. It would be interesting to learn if mutants of such bacteria that are defective in biofilm formation on solid substrates are also impaired in their ability to colonize the neuston. The recent oil spill in the Gulf of Mexico obviously is relevant to this topic. Just as “fertilization” of areas where oil reaches the shore can accelerate bioremediation by supporting luxuriant microbial growth (including alkane degraders), it would be no surprise to learn that the bacterioneuston in the area of the oil spill has undergone a change in population structure and function while taking advantage of the oil as an unexpected source of energy and carbon. I am quite certain that microbiologists are investigating this, and I look forward to learning how the Gulf bacterioneuston responds over time. While an oil spill can cause great damage, it may also yield insights into how marine microbial ecology responds to abrupt change, particularly change precipitated by human actions.

Philosophically, it is awe inspiring to think of the entire surface of the oceans as a nearly two-dimensional biofilm spanning the globe, a world apart from the water column beneath. This floating world beckons to us to explore the population structure of the marine bacterioneuston living therein. With the knowledge gained, we may be able to assist Nature in what we perceive as the natural “clean up” processes that are the microbial world’s response to nutritional and environmental change.

In his novel, Solaris, the late science fiction writer Stanislaus Lem described a world-spanning ocean that was itself sentient. I am not prepared to go quite that far with this concept of a thin, ocean-spanning biofilm, even though microbial communication surely takes place therein. Nevertheless, this concept certainly has made me look at the expression of pouring oil on troubled waters in a new light. Perhaps we need a new aphorism for peace making, one that encourages the formation of robust surface biofilms to minimize disruptions!


Mark O. Martin is an Associate Professor of Biology at the University of Puget Sound in Tacoma, Washington, and an Associate Blogger for Small Things Considered. He remains an unrepentant microbial supremacist.

Cunliffe M, & Murrell JC (2009). The sea-surface microlayer is a gelatinous biofilm. The ISME journal, 3 (9), 1001-3 PMID: 19554040


The idea of developing oil-degrading microbes in the laboratory and applying them to oil spills sounds appealing. But it appears as if that approach does not work well, for a very straightforward reason: organisms must be adapted to the environment in which you release them, if you expect them to proper and grow. Here is a short reference:

In the "olden days," agricultural scientists would find "better" strains of Rhizobium that more efficiently fixed nitrogen. When those strains were applied to fields, they didn't work as well as had been hoped. This is because. again, the new bacteria could not compete in that particular environment. If soil is a complex environment, imagine the bacterioneuston!

This is why most folks involved in bioremediation try to encourage the desired microbes to prosper from the extant population.

But there are also people working of better understanding that process....

In all that I've read since the horrific BP spill in the Gulf, I was surprised that the engineered pseudomonas bacteria of Ananada Chakrabarty  - the first living organism to be patented (after decision by US Supreme Court in June, 1980) - played no role.  This was a huge event in patent law - but in the practical world of its intended application...nothing?

Intrinsic bioremediation of petroleum hydrocarbon (PHC) plumes (which includes both aliphatic and aromatic PHCs) in soil and groundwater are well documented. This is the primary reason that gasoline has not been a significant threat to drinking water until the addition of MTBE, which is not aggressively biodegraded by naturally occurring bacteria. The near-source core of most PHC plumes shows evidence of methanogenesis. The primary bioproduct, however, is CO2. After all of the dissolved O2 is consumed, the bugs use NO3 and SO4 and other alternate electron acceptors. The visual effects on soils are striking where uncontaminated soils are typically an orange brown, the strongly reducing conditions change the valence state of iron and other metals producing various shades of green and blue soil.

If a similar mechanism occurs in the ocean with a crude oil spill, then one would expect that general wet chemistry tests from samples within and outside the impact zones would reveal a geochemical fingerprint that could be plugged into stoichiometric models to calculate the mass of oil bio-transformed.

True enough, Nathan.

Also, for folks interested in what happens to oil *beneath* the water (the infamous "oil plumes"), MIcrobeWorld linked to this ACS article:

Very much worth your time. Andreas Teske is a truly excellent microbiologist, and I am glad he is on the case. Once again, one person's waste is another microbe's feast?

According to its Wikipedia page, BP also took delivery of millions of gallons (60kgal/d) of another dispersant, brand name Dispersit, of entirely different composition and toxicity. We don't know how much BP used of each, or how.

It seems odd that the toxicity of these substances is only measured against arthropods, two of them: shrimp and silverfish.

Eric, these are great questions. At the recent General Meeting of the American Society for Microbiology, there were some thoughts on microbes versus oil. In fact, STC had a link:

Notice Ron Atlas' comment that adding bacteria isn't as effective as allowing the localized population explosion of naturally occurring hydrocarbon degraders.

I hope that scientists sampled the neuston throughout the process, and if nothing else, froze the samples away for later analysis. It's important work, and quite interesting. Who lives in that very thin layer, and what they are doing there, is very, very interesting.

Is there anyone doing the required calculations to determine if the bacterioneuston would even have been capable of handling the sudden influx of food? Based on the current results we are seeing, I think the answer is unequivocal yes, but would be interested in seeing such a calculation.

I think it is especially instructive in this instance that the surface oil seemed to reach a maximum extent but then started to shrink and eventually disappear. In other words, it appears the bacterioneuston was initially overwhelmed with the influx of new nutrients. But given the time, was able to battle back through both time and space, i.e. population explosion and impacted volume of water.

It is probably too late, but it would also have been interesting to see if the bacterioneuston expanded vertically in the spill zone from the one millimeter described in the article to several millimeters.

BTW caught the link from Instapundit. Enjoyed the article very much especially as the ramifications for ongoing operations in the world are profound, i.e. deep water drilling is environmentally safer as most of the oil is "eaten" by the ocean.

After reading similar types of analysis elsewhere, ie the "bugs" ate it, I think a more rigorous analysis is warranted to even determine if a "biomass explosion" could have handled the volume of oil spilled during the time of the spill.

Another interesting line of query would be what the make up of the oil was that made it to shore. Was it a function of timing and the bacterioneuston could not process the oil in time or is it a composition of chemicals not easily broken down by the bacterioneuston?

Nathan, I think they are using this as a dispersant in the Gulf, or were using it:

Two thoughts: (i) if oxygen is necessary to help degrade the oil (not always true), keeping droplets in suspension may not be the right approach (but it would look better than to have great ugly slicks at the surface?), and (ii) it may provide yet another microbial feast depending on the composition of the substance.

When I used to work in industry, we would add surfectants to agar before pouring the plates, so bubbles wouldn't form. But the "debubbling agent" definitely appeared to impact colony size (I never did growth curves and such in liquid).

I have a sinking feeling that this may have been about cosmetic value, not cleaning things up per se. But I am *not* a petroleum engineer, nor a marine biologist.

This is a little off topic, but I wonder about the effect of the millions of gallons of dispersants mixed into the oil on the microbes that are expected to eat the oil. The dispersant is said to degrade in air, but not deep under water. Is there anything that can be expected to eat it? Does it poison the bugs that are supposed to eat the oil?

What nice comments, folks!

Steve, I think it is likely that warmer weather would encourage faster microbial growth in general. Even obligate psychrophiles are not exactly speed-demons with respect to growth rate.

Kevin, that was a very interesting link. Something I didn't have time to discuss was the role that "layers" at the surface of liquids have on gas exchange and the like. Just as people are rightly concerned about oil slicks in this regard, it may well be that microbes are adept at dealing---and perhaps taking advantage of--- this "boundary." I don't have a link handy, but I have seen images of methanogens that live in mud, producing methane anaerobically. But to use methane, organisms require oxygen. So the methanotrophs live at the surface, and generate a floating "mat" of EPS that appears just like plastic wrap. This traps the bubbles of methane in juxtaposition to the required oxygen, where the methanotrophs can best metabolize it. The Small Masters are clever, and subtle.

Garrettc, absolutely. Pretty much anywhere there is liquid water (and some kind of redox potential), microbial life will eke out a living. By better understanding the natural processes, perhaps we can assist Nature in cleaning up our own messes?

I recommend the fine book "Impossible Extinction" by Charles Cockell:

This book truly got me thinking about Microbial Supremacy. What we view as "bad" or "toxic," microbes view as opportunity, in the ecological and evolutionary senses of the term.

I just looked up the oil spills that were most memorable for generating nightmare pictures of dead wildlife. They all took place during cold months in medium-high latitudes. Conversely, this oil spill (and the Gulf War aftermath oil spills) took place where it's downright tropical. Relatively few pictures of environmental devastation have come from them. This isn't science, but it raises an interesting question.

Is there something about warm weather that encourages microbes (or something) to chow down on oil slicks?

I recently wrote about pouring oil on troubled waters and the experiments of Ben Franklin regarding this phenomenon if you are interested.

I would imagine that bacteria which use alkanes a food source are present in higher numbers and species diversity in areas with substantial natural oil seepage. That would be the Gulf, off coast of Santa Barbara, the Alaskan waters, to speculate about a few areas. Bacterial colonies have been found in a number of hostile enviornments that have evolved surprising and sophisticated survival schemes. Think about the rich diversity found in the hot springs of Yellowstone, or the hot anaerobic undersea vents. The mechanisms that promote homeostasis on this planet are quite amazing.

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