Microbial mat

A microbial mat consists of several layers, each of which is dominated by specific types of microorganism, mainly bacteria. Although the composition of individual mats varies depending on the environment, as a general rule the by-products of each group of microorganisms serve as "food" for other groups. In effect each mat forms its own food chain, with one or a few groups at the top of the food chain as their by-products are not consumed by other groups. Different types of microorganism dominate different layers based on their comparative advantage for living in that layer. In other words, they live in positions where they can out-perform other groups rather than where they would absolutely be most comfortable — ecological relationships between different groups are a combination of competition and co-operation. Since the metabolic capabilities of bacteria (what they can "eat" and what conditions they can tolerate) generally depend on their phylogeny (i.e. the most closely related groups have the most similar metabolisms), the different layers of a mat are divided both by their different metabolic contributions to the community and by their phylogenetic relationships.

In a wet environment where sunlight is the main source of energy, the uppermost layers are generally dominated by aerobic photosynthesizing cyanobacteria (blue-green bacteria whose color is caused by their having chlorophyll), while the lowest layers are generally dominated by anaerobic sulfate-reducing bacteria.[4] Sometimes there are intermediate (oxygenated only in the daytime) layers inhabited by facultative anaerobic bacteria. For example, in hypersaline ponds near Guerrero Negro (Mexico) various kind of mats were explored. There are some mats with a middle purple layer inhabited by photosynthesizing purple bacteria.[5] Some other mats have a white layer inhabited by chemotrophic sulfur oxidizing bacteria and beneath them an olive layer inhabited by photosynthesizing green sulfur bacteria and heterotrophic bacteria.[6] However, this layer structure is not changeless during a day: some species of cyanobacteria migrate to deeper layers at morning, and go back at evening, to avoid intensive solar light and UV radiation at mid-day.[6][7]

Microbial mats are generally held together and bound to their substrates by slimy extracellular polymeric substances which they secrete. In many cases some of the bacteria form filaments (threads), which tangle and thus increase the colonies' structural strength, especially if the filaments have sheaths (tough outer coverings).[2]

This combination of slime and tangled threads attracts other microorganisms which become part of the mat community, for example protozoa, some of which feed on the mat-forming bacteria, and diatoms, which often seal the surfaces of submerged microbial mats with thin, parchment-like coverings.[2]

Marine mats may grow to a few centimeters in thickness, of which only the top few millimeters are oxygenated.[8]

Underwater microbial mats have been described as layers that live by exploiting and to some extent modifying local chemical gradients, i.e. variations in the chemical composition. Thinner, less complex biofilms live in many sub-aerial environments, for example on rocks, on mineral particles such as sand, and within soil. They have to survive for long periods without liquid water, often in a dormant state. Microbial mats that live in tidal zones, such as those found in the Sippewissett salt marsh, often contain a large proportion of similar microorganisms that can survive for several hours without water.[2]

Microbial mats and less complex types of biofilm are found at temperature ranges from –40 °C to +120 °C, because variations in pressure affect the temperatures at which water remains liquid.[2]

They even appear as endosymbionts in some animals, for example in the hindguts of some echinoids.[9]

Wrinkled Kinneyia-type sedimentary structures formed beneath cohesive microbial mats in peritidal zones.[10] The image shows the location, in the Burgsvik beds of Sweden, where the texture was first identified as evidence of a microbial mat.[11]

Kinneyia-like structure in the Grimsby Formation (Silurian) exposed in Niagara Gorge, New York

Blister-like microbial mat on ripple-marked surface of a Cambrian tidal flat at Blackberry Hill, Wisconsin

Microbial mats use all of the types of metabolism and feeding strategy that have evolved on Earth—anoxygenic and oxygenic photosynthesis; anaerobic and aerobic chemotrophy (using chemicals rather than sunshine as a source of energy); organic and inorganic respiration and fermentation (i..e converting food into energy with and without using oxygen in the process); autotrophy (producing food from inorganic compounds) and heterotrophy (producing food only from organic compounds, by some combination of predation and detritivory).[2]

Most sedimentary rocks and ore deposits have grown by a reef-like build-up rather than by "falling" out of the water, and this build-up has been at least influenced and perhaps sometimes caused by the actions of microbes. Stromatolites, bioherms (domes or columns similar internally to stromatolites) and biostromes (distinct sheets of sediment) are among such microbe-influenced build-ups.[2] Other types of microbial mat have created wrinkled "elephant skin" textures in marine sediments, although it was many years before these textures were recognized as trace fossils of mats.[11] Microbial mats have increased the concentration of metal in many ore deposits, and without this it would not be feasible to mine them—examples include iron (both sulfide and oxide ores), uranium, copper, silver and gold deposits.[2]

Microbial mats are among the oldest clear signs of life, as microbially induced sedimentary structures (MISS) formed 3,480 million years ago have been found in western Australia.[2][12][13] At that early stage the mats' structure may already have been similar to that of modern mats that do not include photosynthesizing bacteria. It is even possible that non-photosynthesizing mats were present as early as 4,000 million years ago. If so, their energy source would have been hydrothermal vents (high-pressure hot springs around submerged volcanoes), and the evolutionary split between bacteria and archea may also have occurred around this time.[14]

The earliest mats were probably small, single-species biofilms of chemotrophs that relied on hydrothermal vents to supply both energy and chemical "food". Within a short time (by geological standards) the build-up of dead microorganisms would have created an ecological niche for scavenging heterotrophs, possibly methane-emitting and sulfate-reducing organisms that would have formed new layers in the mats and enriched their supply of biologically useful chemicals.[14]

It is generally thought that photosynthesis, the biological generation of energy from light, evolved shortly after 3,000 million years ago (3 billion).[14] However an isotope analysis suggests that oxygenic photosynthesis may have been widespread as early as 3,500 million years ago.[14] The eminent researcher into Earth's earliest life, William Schopf, argues that, if one did not know their age, one would classify some of the fossil organisms in Australian stromatolites from 3,500 million years ago as cyanobacteria, which are oxygen-producing photosynthesizers.[15] There are several different types of photosynthetic reaction, and analysis of bacterial DNA indicates that photosynthesis first arose in anoxygenic purple bacteria, while the oxygenic photosynthesis seen in cyanobacteria and much later in plants was the last to evolve.[16]

The earliest photosynthesis may have been powered by infra-red light, using modified versions of pigments whose original function was to detect infra-red heat emissions from hydrothermal vents. The development of photosynthetic energy generation enabled the microorganisms first to colonize wider areas around vents and then to use sunlight as an energy source. The role of the hydrothermal vents was now limited to supplying reduced metals into the oceans as a whole rather than being the main supporters of life in specific locations.[16] Heterotrophic scavengers would have accompanied the photosynthesizers in their migration out of the "hydrothermal ghetto".[14]

The evolution of purple bacteria, which do not produce or use oxygen but can tolerate it, enabled mats to colonize areas that locally had relatively high concentrations of oxygen, which is toxic to organisms that are not adapted to it.[17] Microbial mats would have been separated into oxidized and reduced layers, and this specialization would have increased their productivity.[14] It may be possible to confirm this model by analyzing the isotope ratios of both carbon and sulfur in sediments laid down in shallow water.[14]

The last major stage in the evolution of microbial mats was the appearance of cyanobacteria, photosynthesizers which both produce and use oxygen. This gave undersea mats their typical modern structure: an oxygen-rich top layer of cyanobacteria; a layer of photosynthesizing purple bacteria that could tolerate oxygen; and oxygen-free, H₂S-dominated lower layers of heterotrophic scavengers, mainly methane-emitting and sulfate-reducing organisms.[14]

It is estimated that the appearance of oxygenic photosynthesis increased biological productivity by a factor of between 100 and 1,000. All photosynthetic reactions require a reducing agent, but the significance of oxygenic photosynthesis is that it uses water as a reducing agent, and water is much more plentiful than the geologically produced reducing agents on which photosynthesis previously depended. The resulting increases in the populations of photosynthesizing bacteria in the top layers of microbial mats would have caused corresponding population increases among the chemotrophic and heterotrophic microorganisms that inhabited the lower layers and which fed respectively on the by-products of the photosynthesizers and on the corpses and / or living bodies of the other mat organisms. These increases would have made microbial mats the planet's dominant ecosystems. From this point onwards life itself produced significantly more of the resources it needed than did geochemical processes.[18]

Oxygenic photosynthesis in microbial mats would also have increased the free oxygen content of the Earth's atmosphere, both directly by emitting oxygen and because the mats emitted molecular hydrogen (H₂), some of which would have escaped from the Earth's atmosphere before it could re-combine with free oxygen to form more water. Microbial mats thus played a major role in the evolution of organisms which could first tolerate free oxygen and then use it as an energy source.[18] Oxygen is toxic to organisms that are not adapted to it, but greatly increases the metabolic efficiency of oxygen-adapted organisms[17] — for example anaerobic fermentation produces a net yield of two molecules of adenosine triphosphate, cells' internal "fuel", per molecule of glucose, while aerobic respiration produces a net yield of 36.[19] The oxygenation of the atmosphere was a prerequisite for the evolution of the more complex eukaryote type of cell, from which all multicellular organisms are built.[20]

Cyanobacteria have the most complete biochemical "toolkits" of all the mat-forming organisms: the photosynthesis mechanisms of both green bacteria and purple bacteria; oxygen production; and the Calvin cycle, which converts carbon dioxide and water into carbohydrates and sugars. It is likely that they acquired many of these sub-systems from existing mat organisms, by some combination of horizontal gene transfer and endosymbiosis followed by fusion. Whatever the causes, cyanobacteria are the most self-sufficient of the mat organisms and were well-adapted to strike out on their own both as floating mats and as the first of the phytoplankton, which forms the basis of most marine food chains.[14]

The time at which eukaryotes first appeared is still uncertain: there is reasonable evidence that fossils dated between 1,600 million years ago and 2,100 million years ago represent eukaryotes,[21] but the presence of steranes in Australian shales may indicate that eukaryotes were present 2,700 million years ago.[22] There is still debate about the origins of eukaryotes, and many of the theories focus on the idea that a bacterium first became an endosymbiont of an anaerobic archean and then fused with it to become one organism. If such endosymbiosis was an important factor, microbial mats would have encouraged it. There are two possible variations of this scenario:

• The boundary between the oxygenated and oxygen-free zones of a mat would have moved up when photosynthesis shut down at night and back down when photosynthesis resumed after the next sunrise. Symbiosis between independent aerobic and anaerobic organisms would have enabled both to live comfortably in the zone that was subject to oxygen "tides", and subsequent endosymbiosis would have made such partnerships more mobile.[14]
• The initial partnership may have been between anaerobic archea that required molecular hydrogen (H₂) and heterotrophic bacteria that produced it and could live both with and without oxygen.[14][23]

Microbial mats from ~1,200 million years ago provide the first evidence of life in the terrestrial realm.[24]

Before:

After:

Sessile organism
anchored in mat

Animal grazing
on mat

Animals embedded
in mat

Animals
burrowing
just under
mat

    =Microbial mat

Firm, layered, anoxic, sulphidic substrate

Animals moving on / in
surface of sea-floor

Loose,
oxygenated
upper substrate
with
burrowing
animals

Before and after the Cambrian substrate revolution

The Ediacara biota are the earliest widely accepted evidence of multicellular "animals". Most Ediacaran strata with the "elephant skin" texture characteristic of microbial mats contain fossils, and Ediacaran fossils are hardly ever found in beds that do not contain these microbial mats.[25] Adolf Seilacher categorized the "animals" as: "mat encrusters", which were permanently attached to the mat; "mat scratchers", which grazed the surface of the mat without destroying it; "mat stickers", suspension feeders that were partially embedded in the mat; and "undermat miners", which burrowed underneath the mat and fed on decomposing mat material.[26]

In the Early Cambrian, however, organisms began to burrow vertically for protection or food, breaking down the microbial mats, and thus allowing water and oxygen to penetrate a considerable distance below the surface and kill the oxygen-intolerant microorganisms in the lower layers. As a result of this Cambrian substrate revolution, marine microbial mats are confined to environments in which burrowing is non-existent or negligible:[27] very harsh environments, such as hyper-saline lagoons or brackish estuaries, which are uninhabitable for the burrowing organisms that broke up the mats;[28] rocky "floors" which the burrowers cannot penetrate;[27] the depths of the oceans, where burrowing activity today is at a similar level to that in the shallow coastal seas before the revolution.[27]

Although the Cambrian substrate revolution opened up new niches for animals, it was not catastrophic for microbial mats, but it did greatly reduce their extent.