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The Microbial Loop Oceanography or collective redistirbution of any portion of this article by photocopy machine, reposting, or other means is permitted only with the approval of The approval Oceanography portionthe ofwith any permitted articleonly photocopy by is of machine, reposting, this means or collective or other redistirbution This article has This been published in A S ea of M icrobe S > SecTion II. IdeaS, ConcepTS, and ParadiGMS > CHapTer 2. THE Microbial Loop Oceanography The Microbial Loop journal of The 20, NumberOceanography 2, a quarterly , Volume BY L AWrence R . PomeroY, PETer J. leB. WilliamS, FarooQ AZam, and JOHN E. Hobbie I presume that the numerous lower pelagic animals persist on the infusoria, which are known to abound in the open ocean: but on what, in the clear blue water, do these infusoria subsist? – Charles Darwin (1845) Answering Charles Darwin’s prescient in the vast oligotrophic blue water where solved organic molecules from seawater question has taken us nearly two cen- they are the dominant autotrophs. as well as organic particles that they turies. Only in recent decades have We now know that every liter of “clear “digest” with enzymes. Some bacteria S ociety. Copyright 2007 by The 2007 by Oceanography Copyright ociety. methods and concepts been developed blue water” is teeming with a billion and archaea oxidize inorganic chemicals to explore the significance of microbes microbes—bacteria, viruses, and pro- for energy, and the carbon they fix into in the ocean’s web of life. Bacteria in tists—far exceeding all multi-cellular organic matter serves as basis for food aquatic ecosystems were first recognized metazoa in abundance, biomass, meta- webs in diverse ecosystems, including for their role in the decomposition of bolic activity, and genetic and biochemi- some in seemingly uninhabitable envi- organic material and the remineraliza- cal diversity. Their struggle for survival ronments. The “smoke” coming from tion of inorganic nutrients, a role that is manifest in a web of microbial life, hot vents on the seafloor may even con- S only became fully accepted in the 1980s. the microbial loop, which is function- tain some bacteria and archaea (Box 1). reproduction, systemmatic Republication, article use for research. and this copy in teaching to granted rights All reserved. is ociety. Permission S Their importance as photosynthetic pro- ally intertwined with the more familiar Earth’s ocean is most certainly a sea of ociety. ducers of organic matter became evident food web of plants, herbivores, and car- microbes; without them it would be a S end all correspondence to: [email protected] or Th e [email protected] Oceanography to: correspondence all end when so-called blue-green algae were nivores. It channels energy and carbon very different place, less hospitable to all acknowledged as being bacteria, and via bacteria to protozoa (Darwin’s infu- life. Indeed, without the activity of these the microscopic cyanobacterium of the soria), to larger zooplankton such as organisms, the cycles of Nature would genus Synechococcus was discovered to copepods and krill, and on to fishes and very quickly come to a halt. This is not be abundant in the oceans—particularly cetaceans. Indeed, when we eat mahi- the case for higher organisms: whereas mahi, we are the top predator in a food the near extinction of the great whales by LAWrence R. PomeroY (lpomeroy@ web that has some of its beginnings in fishing undoubtedly modified the ecol- uga.edu) is Alumni Foundation Professor the microbial loop. ogy of the Antarctic, it certainly did not Emeritus, Institute of Ecology, University About one-half of the oxygen in every bring it to a stop. of Georgia, Athens, GA, USA. PETer breath we take derives from photosyn- S J. leB. WilliamS is Professor Emeritus, thetic bacteria within the marine micro- MICROBIAL DOMINANCE PO Box 1931, Rockville,ociety, MD 20849-1931, U School of Ocean Sciences, University of bial loop. Bacteria manage to populate Earth’s ocean is estimated to contain Wales, Bangor, UK. FarooQ AZam all parts of the ocean by capturing nutri- 1029 bacteria (Whitman et al., 1998), is Distinguished Professor, Scripps ents and energy from diverse sources. a number larger than the estimated Institution of Oceanography, La Jolla, CA, Photosynthetic bacteria carry out much 1021 stars in the universe. Their great USA. JOHN E. Hobbie is Senior Scholar, of the primary production of organic numerical abundance makes up for their The Ecosystems Center, Marine Biological matter in the central ocean basins. size, typically 0.2–0.6 µm in diameter. Laboratory, Woods Hole, MA, USA. Heterotrophic bacteria capture dis- The total mass of bacteria in the ocean S A. 28 Oceanography Vol. 20, No. 2 exceeds the combined mass of zoo- plankton and fishes. Fish biomass is too BOX 1. THE KindS of MicroorGaniSMS Domain Eukarya small even to show relative to others in Animals Figure 1. The entire microbial food web, Fungi including protozoan microzooplankton, Plants Domain Archaea is typically some five to ten times the Domain Bacteria Ciliates mass of all multicellular marine organ- Microorganisms Flagellates isms (locally, these ratios vary widely). include members The potential metabolic dominance of of many branches of the tree of life, from the microorganisms is even greater than most primitive to the most their biomass would suggest (Figure 2). advanced. What were once Progenote Heterotrophic bacteria have poten- simply called “bacteria” have been tially fierce metabolic rates. For example, separated into two distinct domains, the marine bacterium Pseudomonas Bacteria and Archaea, initially on the basis of differences in their ribosomal RNA W( oese natrigens (now renamed Beneckea natri- and Fox, 1977). Archaea look superficially much like bacteria, but their basic biochemistry gens) can, under optimum conditions, is very different, in some ways more like that of higher organisms (Domain Eukarya), while in other ways it is unique. This is reflected in their position on the Tree of Life. Some archaea divide with a frequency of < 10 min are “extremophiles,” living in very hot water and environments that are very salty, acidic, or per division, a growth potential related alkaline. Others live in extreme cold, in anaerobic mud, or in our anaerobic gut, where they to its surface-to-volume ratio. Whereas outnumber the living cells in our bodies. Protozoa (flagellates and ciliates) and fungi are in the biomass (i.e., volume) sets the ultimate Domain Eukarya along with animals and most of what we call plants. potential for metabolism and therefore growth, all organic and inorganic nutri- ents, oxygen, and waste products have a bacterium the size of a micrometer watts per gram dry weight. Put in more to pass through the cell surface. Thus, would have a metabolic rate a million understandable terms, a mass of B. natri- the metabolism per unit biomass is con- times greater than a human. Other fac- gens equal to 100 humans would have an trolled by the surface-to-volume rela- tors—for example, the rate of DNA energy throughput of about a gigawatt, tionship. In the case of a simple sphere, replication, convoluted surfaces such as much the same as a nuclear power sta- this would be 4πr2/(4/3)r3 = 3/r. In this lungs and gills, the availability of growth tion. This metabolic potential under simple instance, the metabolic rate is substrates—ameliorate the discrepancy optimal circumstances would be rarely, if inversely proportional to the linear rela- somewhat, so that in the case of a human ever, achieved in nature for a number of reasons, notably the low concentration of organic nutrients; but, in principle, it We now know that every liter of “clear blue water” gives bacteria the potential for very rapid is teeming with a billion microbes—bacteria, viruses, response to favorable conditions. This and protists—far exceeding all multi-cellular metazoa is important ecologically in the oceans, in abundance, biomass, metabolic activity, and for if the valuable inorganic nutrients present in particulate organic material genetic and biochemical diversity. produced by plankton are to remain in surface waters and not lost to the ocean tionship between size and metabolism versus this particular bacterium, the dis- depths, there must be rapid colonization that in part gives rise to the allome- crepancy is still about 100,000 fold. The and decomposition of these particles. It tric relationship known as the “mouse energy throughput of B. natrigens divid- may be significant that the bacterium to the elephant” curve. Taken literally, ing every 10 minutes would be 2 kilo- that holds the gold medal for growth rate Oceanography June 2007 29 1000 Adult zooplankton Metazoans Larval zooplankton 100 Proto zoa Bacteria Herbivorous protozoans 10 Inverteb Single-celled Mammal Bacterivorous protozoans Fishes Organisms 1 Algal autotrophs rate s s Bacterial autotrophs 0.1 Annual Production Bacterial heterotrophs 0.01 50 25 25 50 0 75 2 6 10e 10e 10e -2 10e -6 Biomass (% total) Surface area (% total) 10e -10 10e -14 Figure 1. Distribution of biomass and calculated surface area (expressed as a percentage Biomass, Grams of Carbon of total) for planktonic trophic groups in the euphotic zone of the oceans. The biomass value is a geometric mean of the data from various oceanic areas; surface area is calculated Figure 2. Comparison of the production of liv- assuming simple spherical geometry. The total biomass for the plankton is 50 mg C -3m ing organic matter per unit of biomass by dif- and the total surface area is 1.2 m2 m-3. Megaplankton, such as medusae, have not been ferent kinds and sizes of organisms showing the included, although this would not materially change the picture. Compiled from Ducklow relatively high productivity per unit weight by (1999), Pomeroy (2004), and Robinson and Williams (2005) microorganisms.
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