Coating matters in the ‘invisible sea’: Biofilms, marine snow and bioengineering

(First of two parts)

Fish kill reveals invisible forces

In February 2002, after many months of dry and sunny weather, people in the province of Pangasinan witnessed a massive fish kill of bangus being raised in pens and net cages in Bolinao. Masses of dead fish discharged into the open water were soon after washed ashore with incoming tides. With a second mass kill of wild fish and shell fish following on the next day, a considerable stretch of the shoreline was to remain for weeks without the living resources which nutrient-rich intertidal flats are usually expected to sustain.

More recently, coastal marine waters, the everlasting domain of fish "hunters," is increasingly shared with fish "farmers." In economic terms, this makes sense, at least in theory. Could Philippine fish farmers eventually enjoy a similarly sustainable resource base as their cousins in the Ifugao Rice Terraces? Ecocatastrophic events like the one in Bolinao may provoke skepticism. On the other hand, large-scale fish farming has just begun, and we have to ask first: What do we really know about energy flow, carrying capacities, about Nature’s pathways of waste disposal and recycling? How can one reliably assess environmental risks?

Growing interest in food supply for ocean fisheries had paved the way for what later evolved as marine science. One of the early milestones in this development was the design of plankton nets to quantify all drifting organisms (plankton) that could be perceived as a source of fish feed. Defined mesh sizes were used to assess and predict fish production in the ocean. Sunlight-driven (photosynthetic) production of phyto-plankton biomass is mainly fueled by inorganic nutrients. As these become rapidly exhausted, their pools must always be replenished. This is achieved in half-cycles of remineralization that are linked with the formation of living biomass. According to early models, most of the dying plankton has to sink to the seafloor first. Here inorganic nutrients will be regenerated and eventually resurface to sunlight-exposed water layers to fuel another round of fish feed production. When the first models for oceanic ecosystems were applied several decades ago, they paradoxically predicted fish stocks would never be sustained due to lack of food, even under the most optimistic (but completely unrealistic) scenario that fish were able to consume 100 percent of the primary (photosynthetic) production. Apparently, these models were too simple. They relied only on the most visible organisms and their most evident functions. 

‘The invisible sea’

At about the same time scientists and the public alike became gradually aware of missing links in the prevailing knowledge. "Invisible sea" became the title of a film that addressed the role of the microscopically small organisms. Until then, public interest had shunned this hidden and hardly imaginative aspect of marine ecology. Three decades later, marine microbiology has now made huge leaps forward. Meanwhile, molecular genetics enable us to identify microorganisms directly in environmental samples, no tedious cultivation required any more. The 99 percent majority of bacteria that used to evade most sophisticated isolation and cultivation attempts, can at least be tracked down by their genomic signatures. But how has marine microbial ecology changed our perception of fish feed production and fisheries in the ocean? Which lessons have ecosystem modelers been taught? And, above all, how can prokaryotic microbes, these smallest forms of life and direct descendants of the oldest creatures on earth, be involved in the control of life-sustaining processes in the oceans? Could microbes eventually hold a key to sustainable food supply in the ocean? 

Excess fish feed and feces undergoing "enzymatic burning" (respiration) with the help of dissolved molecular oxygen will rapidly deplete the dissolved oxygen in the water column, and even more so, at sediment surfaces on which sinking detritus particles are deposited. This does not mean, however, that recycling or remineralization of organic matter would have to stop, when dissolved oxygen pools have been exhausted. A sequence of alternative pathways replacing oxygen-dependant respiration will be at hand. In the sea environment, the most sustainable recycling pathway for organic matter under oxygen depletion depends on sulfate as an abundant component of seawater salts.

Organic matter recycling via this so-called "sulfate respiration" of marine microbes produces hydrogen sulfide, an easily recognized component with the smell of rotten eggs. Hydrogen sulfide (H2S) is toxic to most animals living in the sea, unless they can manage to produce detoxifying compounds binding it. Most importantly, this toxicant also binds heavy metals. By doing so, it helps to deposit and to detoxify another group of environmental toxicants. In oxygen-rich waters hydrogen sulfide will disappear rapidly. Therefore, clams, crabs and other sediment-inhabiting animals can survive in hydrogen sulfide-rich sediments so long as they manage to irrigate their surroundings with water containing oxygen. Only permanently high rates of hydrogen sulfide production will eventually erase sediment-inhabiting communities. 

Bioengineering at the seafloor

Sediment-dwelling creatures are instrumental to the entire process of organic matter recycling, for many of them work as very effective bioengineers by producing a multitude of tubes, burrows and other structures with aerated (oxidized) interfaces. At these interfaces microbial biofilms are forming: structured communities of microbes that are imbedded in a sticky matrix of (polysaccharide and protein) biopolymers. These prime sites of mineralization dispose of immobilized biocatalysts (ectoenzymes) that are needed to degrade large organic molecules. These biofilms constitute crucial relais stations for organic matter recycling. Where the seafloor has been purged of its sediment-dwelling fauna of bioengineers by excessive production of hydrogen sulfide, those biofilms will become defunct. This means: microbial recycling of organic matter will be deprived of the mediating role of fauna-made biofilms.

This scenario can be observed on the seafloor below excessively fed fish cages in Bolinao Bay (Pangasinan). Where hydrogen sulfide seeps out of the sediment and mixes with traces of oxygen in the water, a niche is created that attracts the filaments of hydrogen sulfide oxidizing bacteria. These giants in the world of microbes can create thick yellowish-white lawns covering the seafloor: the color stems from elemental sulfur, an oxidation product of hydrogen sulfide that is stored in the filaments. These sulfide-oxidizing microbial lawns initiate the restoration of the sediment as a residential area for bottom-living animals. As a "hot spot" of organic matter recycling, an ecologically sound seafloor is virtually perforated with the aerated burrows. Their biofilm-coated walls are housing the microbe-driven machinery of "biochemical "relais stations" as required for organic matter recycling. (To be concluded)

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Wolfgang T. Reichardt, Ph.D. in Botany, is a research professor (DAAD-Lectureship) at the UP Marine Science Institute, Diliman, Quezon City. His research interests are in marine microbial ecology, biogeochemical recycling and mariculture. Send comments and queries to wtreichardt@yahoo.com.