Abstract and Keywords
This chapter is concerned with the landscapes that were still formed in part and were occupied by microbial masters. It limits the discussion to specific temperate-zone aquatic communities of oolitic limestone producers and metalworkers that shape certain underwater sedimentary deposits of iron and manganese. This chapter believes that denizens of the microcosm in community, bacteria, succeeded and supplemented by protoctists and animals, have built homes of some kind, supported themselves by “farming,” and decorated and protected their turf with architectural structures of their own making ever since the anoxic Archean eon.
Congratulating ourselves on our upright stance, our big brains, and our language skills, we consider ourselves the most “evolved” species. But bacteria exceed us in chemical (metabolic) abilities and in importance in distributing the chemical elements in the biosphere. They also build many intricate structures—including, from one way of looking at it, our bodies. Here Krumbein and Asikainen explore another kind of architecture made by collectives of microbes.
Conscious human architecture is considered one of the high points of human civilization. Arches are also built by termites, however, and microbes work manganese and other metals, as well as limestone and other minerals, into functional and beautiful dwellings. Microbial mats from flat, laminated Microcoleus chthonoplastes-dominated communities on the shore of the North Sea in northern Germany were grown in the laboratory. They spontaneously generated balloon-shaped protein-lipid exudates 1–5 millimeters in diameter. When these were subjected to ordinary periodic light and temperature alterations with wet-dry cycles, at first they formed balloon-shaped scums that most ambient bacteria were unable to penetrate. These “mini-balloons” floating in the mat mucus or the water column above the laminated mat communities. The mini-balloons were first colonized by one species of filamentous cyanobacteria (Phormidium hendersonii). A common diatom, Navicula perminuta, glided into the ruptures made by Phormidium and then reproduced inside to fill up the balloon. Five of a total of 11 to 13 strains of heterotrophic bacteria were detected inside the balloon. Most of these bacteria have been grown by themselves in pure culture. Their DNA has been sequenced. Spontaneous calcification occurred and ooids (uniform spherical grains of carbonate sand) were released from the ruptured “balloon skins” in approximately half of 350 cases studied. Those that failed to calcify (p.64) (harden) and release ooids simply disintegrated. These released organic rather than mineralized contents that could not be further studied.
In the second case, a field of concentrically laminated iron-manganese nodules was found at a depth of 10 meters in fresh cold water off the ramp of an abandoned logging camp at the Second Connecticut Lake in Pittsburg, New Hampshire. (See color plate I.) Though the associated bacteria have not yet been identified, the growth pattern from a field of “cow pies” that extend to form a continuous pavement, the presence of a nepheloid biofilm replete with many forms of heterotrophic bacteria, and the laminae suggest that these nodules are a form of rock constructed by microbes, i.e., a microbialite (figure 6.1). In a manner reminiscent of other well-studied stromatolitic communities in the geomicrobiological literature, these sedimentary structures, the intertidal marine oolites, and the submerged freshwater iron manganese nodules form temporary biogenic dwellings for their communities of microbial inhabitants.
Based on our own research and our acquaintance with the geomicrobiology literature, we posit that specific groups of organisms—among
The probability that any planet has the temperature, pressure, and aqueous conditions that permit the biochemistry of life has been called a “life window factor” (Krumbein 2008). Julius Robert von Mayer, one of the founders of the science of chemical thermodynamics, wrote the following in his 1845 book Die organische bewegung in ihrem zusammenhange mit dem stoffwechsel:
Nature posed itself the task to catch light waving from Sun to Earth in its flight and to store this most motile of all forces in a solid form. To achieve this, nature covered Earth with the organisms of life that incorporate the sunlight and use this force to produce a continuous sum of chemical differences. (translation by W. E. Krumbein)
We suggest that interspecific sensory and coordinated physiological activity (“consciousness,” as explained in this book, and “design,” as explained in Turner 2007) are required for the construction of adequate and persistent “homes.” One example is the coordination of sensory input, photo-autotrophic metabolism, and chemo-autotrophic metabolism in microbial communities that is required for transformation from two-dimensional flat laminae at environmental gradient surfaces (water-air, gravitational, organic chemical, and so forth) to form mineralized three-dimensional laminated biofilms (such as stromatolites). Further development into spheres and towers that induce oolites, pisolites, oncolites, and 6-meter-tall fluted Namibian termite mounds or Amazonian tree-top ant dwellings (Wilson 1991) requires far more detailed analysis. However, it is likely that “mindful” coordination of behavior, growth, metabolic, and genetic activities underlies such successful three-dimensional architectures as the magnetic termite mounds found in Australia, which are flat-sided like the tail plane on an aircraft and are aligned on a north-south axis to minimize the midday heat. Houses, nests, sheds, barns, food-storage structures, and other typical products of conscious organization involve coordinated activity by both (p.66) conspecific populations and members of communities of species that, genetically, are related only remotely. Making a barn, to take an obvious example, requires not only humans but also trees. Here we limit our discussion to specific temperate-zone aquatic communities of oolitic limestone producers and metalworkers that shape certain underwater sedimentary deposits of iron and manganese.
As was summarized in the first paragraph of this chapter, ooids coordinate different genera and species of organisms into a logical, mindful, oolitic dwelling (Brehm et al. 2006; Krumbein 2008; Krumbein et al. 2003). The players are Phormidium sp., a cyanobacterium; Navicula perminuta, a diatom; and some less conspicuous chemo-organotroph bacteria, eleven in all, of which five are well-defined named taxa. These thirteen individual participants cooperate using all senses: chemo-autotrophy, mechano-sensitivity, and photo-autotrophy (Brehm et al. 2006). First they need to reach a specific minimal number of individuals within the combined total population. Whether it is the larger associates (diatoms) or the smaller but more numerous bacteria that direct production and lithification remains unknown; most likely all are involved. In laboratory experiments, a chemical substance is generated within the laminated biofilm. The substance differentiates between higher and lower quantities of energy, carbon, and other sources. A complex film begins to be produced. Shaped as a sphere, a new layer or other repeat pattern not unlike the initial cells of a butterfly wing starts to grow. Then these nine to fourteen different types of organisms react to the substance, which in this context behaves as a signal or pheromone message. The cyanobacterial filament glides toward the spherically organized mini-balloon and, if successful, penetrates the pellicle. Then the diatoms and heterotrophic bacteria accompany gliding cyanobacteria and their photosynthetic exudate. Together they penetrate the spherical barrier created by the community (figure 6.2). Inside the sphere a community pattern is observed by light and electron microscopy. Within the yellowish chemical globe several types of heterotrophic bacteria arrange themselves into a palisade. A tightly coiled layer toward the center contains the filamentous cyanobacterium Phormidium hendersonii. (See plate II.) CO2-removing phototrophic and oxygenic cyanobacteria concentrate in the center of the translucent sphere, where they reproduce rapidly by cell division. They form multilayered rough or smooth spheres, some of which eventually solidify and calcify to form an organic-coated ooid. (See plate II.) A two-dimensional layered community transforms in this special way and becomes a spherical one, which creates its own (p.67)
Not all organisms have such mindful organization. In our second example, ferromanganese nodules, the structures are a sign that organisms inhabit the environment. These microbialites are traces of microbial activity and, like ooids, are a product of the chemical gradient in the environment. Although the microbes that facilitate growth of nodules in the Second Connecticut Lake are not yet named and classified, we can extrapolate from analyses of comparable freshwater nodules in Oneida Lake in New York (Beliaev et al. 2002). Nodule growth is associated with the presence of Shewanella oneidensis, a Gram-negative heterotrophic bacterium that generates and removes intracellular iron and manganese oxides (Myers and Nealson 1988). Cyanobacteria, also present because of their phototrophic obligate oxygenesis, produce extracellular oxides of iron and manganese. The oxides form as by-products of free metal ions in solution. The nodule community nucleates the laminated sediments on solid substrates (e.g., rocks, sand grains, mud balls, even glass bottles).
In the Second Connecticut Lake (in New Hampshire, at the headwaters of the Connecticut River drainage system, which travels 655 kilometers to Long Island Sound), nodules are limited to an area of 100 square meters in the central western portion of the lake bottom at depths between 3 and 5 meters (Asikainen and Werle 2007). The hard but friable, generally laminated sediments display a wide variety of nodule morphologies in the small area. Most conspicuous and abundant are convex plate-like structures found in both “up” and “down” positions (figure 6.3A). At least three other nodule morphotypes supplement the plate-like nodules that form concentric rings around a nucleus: pavements, cup-shaped (〈2 cm), and lattices. Underwater pavements derive their name from the continuous “sidewalk” formed by the growth of a porous pustular layer (1–2 cm thick) on the surface of plate-like nodules. In at least two localities, nodules join together into a single cohesive unit—a pavement (figure 6.3B). Small cup-shaped forms have the concentric ring pattern of the plates but lack an obvious central nucleus (figure 6.3C). Lattice structures, also without a central nucleus or concentric rings, have conspicuous voids throughout. They contain randomly distributed pebbles that range in size from small to coarse (figure 6.3D).
Does ferromanganese nodule formation fit the idea of mindful organization? The details of modular “home structure” that corals (animals) or foraminifera (protoctists) construct are more intricate, yet the microbial community influences the size, shape, and durability of sediments within limited volumes in ways that are unprecedented in the abiotic geologic record (Schopf 2006).
Might spherical ooids show, by contrast with laminated nodules, the first signs of mindful community interaction? Who knows? In “home-building,” including great height, humidification, temperature and solar radiation modulation, mineral and organic foodstuff storage, and defense systems, human achievements show continuity with microbial and other animal ingenuity over eons.
Bacteria began the same building trends: houses, gardens with fungal or plant crops in rows, tending of hedges and agricultural plots. We infer that denizens of the microcosm in community, bacteria, succeeded and supplemented by protoctists and animals, have built homes of some kind, supported themselves by “farming,” and decorated and protected their turf with architectural structures of their own making ever since the anoxic Archean eon (Turner 2000).