A paean to prokaryotes

        "Out of sight, out of mind" is never a good rule by which to live, and it's not a good rule for us to use with regard to the unseen prokaryotic life around us.  Prokaryotes play an immense role in shaping our world, and in shaping ourselves.  To ignore them is both to endanger our health and to fail to understand our world.  This essay attempts to review some of the larger-scale evidence for that claim.

Definitions, standard and otherwise

        What's a prokaryote?  The standard definition is "a single-celled organism in which the cell does not have a nucleus", where a nucleus is an enclosed cluster of DNA.  In old-fashioned terms, "bacteria" was essentially synonymous with "prokaryotes".  In the more modern understanding of life, prokaryotes are divided into two major groups, the Archaea and the Eubacteria.  Of those two, the former name clearly implies antiquity of lineage, whereas the latter rightly or wrongly implies the "true" or "good" bacteria.  As the sketches above show, one could generally say that prokaryotes are simply very small single-celled organisms, whereas eukaryotic cells are larger (although a few very large (~1 mm) bacteria would defy that distinction).

        As one of my graduate students has pointed out, the standard definition of "prokaryote" above is a poor one, because it involves a negative instead of a positive⁰.  As one considers the diversity of prokaryotes implied by the diagram above and the abundance of prokaryotes that we'll consider below, a somewhat more positive, if tongue-in-cheek, definition emerges.  That definition might be "all life on Earth, except for those few strange things that have their DNA enclosed in nuclei in their cells".

Diversity of Prokaryotes I

        Consider diversity from this quantitative perspective: genetic studies of soil estimate that 10 grams of unpolluted soil will typically have 8.3 x 10⁶ different species of "bacteria"¹.  That's almost 10 million species in a very small handful of soil.   Similar studies of bacteria on trees found hundreds of species on the leaves of just one tree, with hundreds of other different species on the leaves of adjacent trees^1a.  For comparison, there are only 4500 species of mammals on the entire Earth, perhaps 10,000 to 20,000 species of birds on the entire planet, and 230,000 species of plants globally^2&3.  Even the most diverse taxon of higher organisms, the insects, boasts only about a million species worldwide².  A measly ten grams of soil has more species of prokaryotes than that!

Diversity of Prokaryotes II

        On the other hand, consider diversity from the qualitative perspective.  All metazoans have just one way to metabolize: they take in O₂ and oxidize organic carbon.  Across all the diversity of animals, that's one form of metabolism, in which O₂ is the electron acceptor.  By contrast, prokaryotes can metabolize using sulfur in SO₄^2-, Fe³⁺,Mn³⁺, nitrogen in NO₃^- and NH₃, and even the carbon of organic matter as electron acceptors.  Some even use oxidized uranium, U⁶⁺, as their electron acceptor, and so they metabolize using a radioactive element that we humans avoid like the plague.  At the chemical level, these various mechanisms of metabolism represent far more diversity among prokaryotes than among all the animals, from nematodes to gazelles, even though we typically think the latter are "diverse".  ⁴

        Likewise consider the chemical ability of organisms to harness inorganic energy.  Animals can't do it at all, and plants can only harness the energy of light by photosynthesis.  Prokaryotes can chemosynthesize, using the energy of inorganic chemicals, as well as photosynthesize⁴, and there are probably are variety of avenues of microbial chemosynthesis.

Environmental Range

        One must also consider the diversity of environments in which prokaryotes live. Let's consider different environmental parameters:

Temperature: Hot springs in Iceland host the bacterium Thermus spp. at temperatures up to 85°C⁵, and ocean vents host the archaea Pyrolobus fumarii at 113°C (235°F), as well as Pyrodictium occultum and Methanopyrus kandleri at 110°C (230°F)⁶.  Strain 121, an Fe-reducer found in hydrothermal vents, flourishes at the 120°C temperatures used in autoclaves and survives at 130°C ⁴.  At the other end of the temperature range, bacteria abound in temperatures down to -2°C on the deep sea floor and below ice sheets, and bacteria can grow on ice cream at -10°C ⁷.

pH: The aforementioned hot springs in Iceland host the bacterium Thermus spp. at pH in excess of 10 ⁵, and cyanobacteria have been observed growing in lakes at pH values of 10 to 11.⁷  In the lab, Nitrobacter and Nitrosomonas have been cultured at pH = 13.⁷  At the other end of the range of acidity, hot springs in Beppu, Japan host the archaeon Sulfolobus shibatae at pH = 3.0 ⁶.

Salinity: Salinity is likewise no issue: bacteria are abundant in fresh water and have been grown in doubly-distilled water ⁷.  On the other hand, bacteria can grow at salinities up to 4 M in molar terms ⁸ and in 4.1 M MgSO₄ ⁷.  They are abundant in saline lakes and notably in the Dead Sea, at salinities of about 300 ppt. ⁷

Pressure: Soil bacteria have been cultivated at a pressure of 0.1 atmospheres (a Mars-like atmospheric pressure) and at pressures of 1000 atmospheres ⁷.

Radiation The bacterium Deinococcus radiodurans can survive extreme doses of ionizing radiation and repair the thousands of resulting breaks in its DNA^8a.

        In addition to these ways of considering environments, it's instructive to note that multiple studies have found prokaryotes in deep sea sediments buried to sub-sea-floor depths of more than 400 meters, in sediments buried as much as 16 million years ago⁹.  Similarly, bacteria that "eat" H₂ and "breath" SO₄^2- in fractures 2.8 km below the Earth surface in South Africa seem to have survived there for something between 3 and 25 million years⁹.

Abundance

        If you're tired of these arguments about diversity, one can also marvel at the sheer number of prokaryotes.  For example, a gram of soil can have 2x10⁹ individual prokaryotic cells, numerically equal to about a third of Earth's entire human population, but in just a single gram of soil ¹⁰.  However, every human is also a prokaryotic wonderland, with about 7 x 10¹³ prokaryotic cells in the average human colon, and they represent about 500 microbial taxa¹⁰.  To put that in perspective: if every one of Earth's 6 x 10⁹ humans could hold 10,000 grains of sand in their cupped hands, the total number of grains of sand held by all Earth's people would equal the number of prokaryotes in your colon.  At a larger scale, the total number of prokaryotes on Earth is estimated at 5 x 10³⁰, a number beyond all comparison¹⁰.

Prokaryotes as Eukaryotic Organelles

        If you're dismissive of the prokaryotic cells in your digestive system and otherwise coating your hands, teeths, tongue, and the like, consider the role of prokaryotes in your own "human" cells, and in every eukaryotic cell.  Biologists acknowledge today that mitochondria, the energy-releasing organelles of eukaryotic cells, are descendents of bacteria that were engulfed in a primitive eukaryote and passed down through generations for at least the last billion years.  Why would we think that?  First, each of the many mitochondria in your cells, and in all eukaryotic cells, carries the DNA of a bacterium, separate from the DNA of the eukaryote.  Secondly, each mitochondrion has a double cell membrane around it, exactly what one would expect if the mitochondrion were engulfed in a fold of the membrane of a larger eukaryote.  The same sort of observations likewise leads to the conclusion that the photosynthesizing chloroplasts of plants are descended from cyanobacteria engulfed by a eukaryote.  Thus all our "higher" eukaryotic life depends on the services of prokaryotic symbionts living within our eukaryotic cells.

Longevity, Individually and Collectively

        The macroscopic organisms with which we're familiar have life spans of weeks to years, and at most a century or so.  Prokaryotes can certainly top that.  A bacterium has been extracted from seawater trapped in a fluid inclusion in salt deposits of Permian age (i.e., an age of about 250 million years).  That bacterium was then cultured, which means that it was not dead when collected after its 250-million-year entombment.  It had thus survived longer than the entire collective age range of mammals and birds.¹¹

        It's of course no surprise that bacteria were present 250 million years ago.  Fossil and geochemical evidence tell us that Earth's earliest life forms were prokaryotes, and that they were present in excess of three billion years ago.  By comparison, all eukaryotic life is a Johnny-come-lately, as the evolutionary history of eukaryotes discussed above would suggest.

Ecological significance

        Prokaryotes provide an essentially ecological service in liberating the nutrients needed for photosynthesis and thus for the sustenance of life.  This is most easily recognized in the ecology of the oceans, where is has long been known that bacteria are critical in liberating nitrogen and phosphorous from organic compounds by oxidizing them to the inorganic forms in which they are nutrients.  More recently we've come to realize that bacteria strip the coatings off particles of biogenic silica to return dissolved silicon to seawater as a nutrient.  Even more recently, research has shown that marine bacteria produce siderophores, iron-bearing organic ligands, that facilitate the photochemical reduction of iron from its biologically useless Fe³⁺ state to its Fe²⁺ state essential to photosynthesis¹².  Dolphins and whales are the photogenic superstars of marine ecology, but they wouldn't exist were it not for prokaryotes.

        The upshot of the ecological services of prokaryotes is that they are essential to the global ecosystem. In that regard, the New York Times quoted Carl Woese, the discoverer of the Archaea, as saying, "It's clear to me that if you wiped all multicellular life-forms off the face of the earth, microbial life might shift a tiny bit . . . If [on the other hand] microbial life were to disappear, that would be it - instant death for the planet."¹³

Summary

        In short, prokaryotes are incredibly abundant, they're remarkably diverse, they're everywhere, they've always been everywhere, and it's a good thing that they're in many places.  Whether you're preparing to eat lunch or preparing to explain any natural process, you ignore them at your peril.

Sources:

⁰Grad Student Julie Fiser's observation was echoed recently by Norman Pace in Nature (v. 441, p. 289, 2006). In response, William Martin and Eugene V. Koonin argued that prokaryotes can be defined positively, rather than negatively, as "cells with co-transcriptional translation on their main chromosomes; they translate nascent messenger RNAs into protein", whereas eukaryotes do not (Nature, v. 442, p. 868, 2006).

¹ Gans, J., et al., 2005, Computational improvements reveal great bacterial diversity and high metal toxicity in soil: Science, v. 309, p. 1387-1390.

^1a Lambais, M.R. et al., 2006, Bacterial diversity in tree canopies of the Atlantic Forest: Science, v. 312, p. 1917.

² Canada's species: http://www.canadianbiodiversity.mcgill.ca/english/species/

³ Mayr, E., 1946, The Number of Species of Birds: Auk, 63: 64-69.

⁴ Nee, S., 2004, More Than Meets the Eye: Nature, v. 429, p. 804-805.
Min, M., Xu, H., Chen, J., and Fayek, M., 2005, Evidence of uranium bioineralization in sandstone-hosted roll-front uranium deposits, northwestern China: Ore Geology Reviews, v. 26, p. 198-206.

⁵ Jakob K. Kristjansson and Gudni A. Alfredsson, 2003, Distribution of Thermus spp. in Icelandic Hot Springs and a Thermal Gradient: Appl. Environ. Microbiol. 45(6): 1785-1789.

⁶ Hiromi Kagawa, 2005, Life in Japan's Acidic Hot Springs: http://www.space.com/searchforlife/seti_hot_springs_050901.html.

⁷ Zajic, J.E., 1969, Microbial Biogeochemistry: New York, Academic Press, 345 p.

⁸Stevenson, J.R., MB202 General Microbiology II lecture on Extreme Habitats: http://www.cas.muohio.edu/~stevenjr/mbi202/extremehabitats202.html

^8aZahradka, K., et al., 2006, Reassembly of shattered chromosomes in Deinococcus radioduras: Nature, v. 443, p. 569-573.

⁹ Schippers, A., et al., 2005, Prokaryotic cells of the deep sub-seafloor biosphere identified as living bacteria: Nature, v. 433, p, 861-864;
Parkes, R.J., et al., 2005, Deep sub-seafloor prokaryotes stimulated at interfaces over geologic time: Nature, v. 436, p. 390-394;
Lin, L.-H., et al., 2006, Long-term sustainability of a high-energy low-diversity crustal biome: Science, v. 314, p. 479-482.

¹⁰abundance: Whitman, W.B., et al., 1998, Prokaryotes: The unseen majority: Proc. Nat. Acad. Sci. USA, v. 95, p. 6578-6583. Diversity: Silverman, N., and Paquette, N., 2008, The right resident bugs: Science, v. 319, p. 734, citing Eckburg, P.B., et al., 2005, Science, v. 308, p. 1635.

¹¹Satterfield, C.L., et al., 2005, New evidence for 250 Ma age of halotolerant bacterium from a Permian salt crystal: Geology, v. 33, p. 265-268; Hanson, B., 2005, Preserved in salt: Nature, v. 308, p. 603.

¹²Barbeau, K., 2006, Photochemistry of organic iron(III) complexing ligands in oceanic systems: Photochemistry and Photobiology, v. 82, p. 1505-1516.

¹³Yardley, W., 2012, Carl Woese Dies at 84; Discovered Life's 'Third Domain': New York Times December 31, 2012 (www.nytimes.com/2013/01/01/science/carl-woese-dies-discovered-lifes-third-domain.html?hpw)

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