14 Aug 2001 17:34 AR AR135-05.tex AR135-05.SGM ARv2(2001/05/10) P1: GDLAnnu. Rev. Microbiol. 2001. 55:105–37Copyrightc° 2001 by Annual Reviews. All rights reservedBIG BACTERIAHeide N. Schulz and Bo Barker JørgensenMax-Planck-Institute for Marine Microbiology, Celsiusstrasse 1, D-28359 Bremen,Germany; e-mail: [email protected]; [email protected] Words prokaryote cell size, diffusion, diffusive boundary layer, chemotaxis,sulfide oxidizing bacteria■ Abstract A small number of prokaryotic species have a unique physiology orecology related to their development of unusually large size. The biomass of bacteriavariesover morethan 10orders ofmagnitude, fromthe 0.2 µmwide nanobacteriato thelargestcellsofthecolorless sulfurbacteria,Thiomargaritanamibiensis,withadiameterof 750 µm. All bacteria, including those that swim around in the environment, obtaintheir food molecules by molecular diffusion. Only the fastest and largest swimmersknown,Thiovulummajus,areable tosignificantlyincrease theirfoodsupply bymotilityand by actively creating an advective flow through the entire population. Diffusionlimitation generally restricts the maximal size of prokaryotic cells and provides aselective advantage for µm-sized cells at the normally low substrate concentrations inthe environment. The largest heterotrophic bacteria, the 80 × 600 µm large Epulo-piscium sp. from the gut of tropical fish, are presumably living in a very nutrient-richmedium. Many large bacteria contain numerous inclusions in the cells that reducethe volume of active cytoplasm. The most striking examples of competitive advantagefrom large cell size are found among the colorless sulfur bacteria that oxidize hydrogensulfide to sulfate with oxygen or nitrate. The several-cm-long filamentous species canpenetrate up through the ca 500-µm-thick diffusive boundary layer and may therebyreach into water containing theirelectron acceptor, oxygen or nitrate. By their ability tostore vast quantities of both nitrate and elemental sulfur in the cells, these bacteria havebecome independent of the coexistence of their substrates. In fact, a close relative, T.namibiensis, can probably respire in the sulfidic mud for several months before againfilling up their large vacuoles with nitrate.CONTENTSTHE SCALE OF LIVING ORGANISMS ..................................106DIFFUSION AND THE SIZE LIMIT OF PROKARYOTES ....................107CHEMOTAXIS .......................................................111THE SEDIMENT-WATER INTERFACE ...................................112BIG BACTERIA ......................................................115ECOLOGICAL NICHES OF BIG BACTERIA ..............................119Holding on in Flowing Water ..........................................119Life in One-Dimensional Opposed Diffusion Gradients ......................121Fast Swimmers and Organized Communities ..............................1230066-4227/01/1001-0105$14.0010514 Aug 2001 17:34 AR AR135-05.tex AR135-05.SGM ARv2(2001/05/10) P1: GDL106 SCHULZ¥JØRGENSENBreaking Through the Diffusive Boundary Layer ...........................124Surviving Anoxia with a Storage Tank of Nitrate ...........................127Monopolizing Substrates by Commuting .................................128Waiting for the Electron Acceptor .......................................130SUMMARY ..........................................................131THE SCALE OF LIVING ORGANISMSWithin the past decade, several uncultured bacteria were consecutively announcedas the largest known prokaryotes: Epulopiscium fishelsoni (3), Beggiatoa sp. (48),and T. namibiensis (83). Over the years, big bacteria have been described as“megabacteria” or “gigantobacteria” or given names such as “Titanospirillum”(20, 30). The current holder of the biovolume record, a chain-forming, sphericalsulfur bacterium, T. namibiensis, was discovered only recently in the sea floor offthe coast of Namibia (83). The cells may reach 750 µm diameter, clearly visibleto the naked eye. They form chains of cells that, due to their light refracting sulfurglobules, shine white on the background of black mud and thus appear as a stringof pearls (Thiomargarita = sulfur pearl).Also the rod-shaped heterotrophic bacterium, Epulopiscium fishelsoni, found infish guts may reach a giant size of 80 µm diameter and 600 µm length (3,10). Thelargest reported Archaea are probably the extremely thermophilic Staphylother-mus marinus, which in culture may occasionally have cell diameters up to 15 µm(19). The smallest prokaryotes are found among both the Archaea and the Eubac-teria. The disk-shaped cells of the archaea, Thermodiscus, have diameters down to0.2 µm and a disk-thickness of 0.1–0.2 µm (87). Under the collective designationof nanobacteria or ultramicrobacteria, a range of cell forms with diameters down to0.2–0.3 µm have been found in both natural samples and cultures (92). Altogether,the biovolumes of prokaryotic cells may cover a range of more than 10 orders ofmagnitude, from <0.01 µm3for the smallest prokaryotic cells to 200,000,000 µm3for the largest.When all living organisms are considered, from bacteria to whales, the sizescale is so vast that it is difficult to comprehend. Whereas the smallest prokaryoticcells are at the resolution of the light microscope, 0.2 µm, the blue whales at theother end of the spectrum may grow to 30 m in length, 8 orders of magnitudelarger than the nanobacteria. The maximum span in biomass between bacteria andwhales is the third power of their difference in size (or somewhat less, becausewhales are not spherical), i.e., 1:1022–23. This is similar to the volume ratio betweenhumans and the earth.It is therefore not surprising that the world, as it appears in the microscale ofbacteria, is also vastly different from the world that we humans can perceive andfrom which we have learned to appreciate the physical laws of nature. These arethe classical laws of Newton relating mass, force, and time with mass movementand flow, and with properties such as acceleration, inertia, and gravitation. Aswe go down in scale and into the aqueous microenvironment of bacteria, these14 Aug 2001 17:34 AR AR135-05.tex AR135-05.SGM ARv2(2001/05/10) P1: GDLBIG BACTERIA 107properties lose their significance. Instead, viscosity becomes the strongest forceaffecting motion, and molecular diffusion the fastest transport. Viscosity affectshow bacteria swim through their aqueous environment, and it affects