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or collective redistirbution other or collective or means this reposting, of machine, is by photocopy article only anypermitted of with portion the approvalOceanography S The of This article has been published in published been This has article A s ea of M icrobe s

> Section II. Ideas, Concepts, and Paradigms

> Chapter 2. The

The Microbial Loop , Volume 2, a quarterlyOceanography 20, Number S The journal of By L awrence R . Pomeroy, Peter J. leB. wILLIA Ms, Farooq Azam, and John E. Hobbie

I presume that the numerous lower pelagic persist on the infusoria, which are known to abound in the open : but on what, in the clear blue , do these infusoria subsist? – (1845)

Answering Charles Darwin’s prescient in the vast oligotrophic blue water where solved organic molecules from question has taken us nearly two cen- they are the dominant . as well as organic particles that they turies. Only in recent decades have We now know that every liter of “clear “digest” with . Some ociety. CopyrightOceanography S 2007 by The methods and concepts been developed blue water” is teeming with a billion and oxidize inorganic chemicals to explore the significance of microbes microbes—bacteria, , and pro- for energy, and the they fix into in the ocean’s web of . Bacteria in tists—far exceeding all multi-cellular serves as basis for food aquatic were first recognized metazoa in , , meta- webs in diverse ecosystems, including for their role in the 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 , a role that is manifest in a web of microbial life, hot vents on the seafloor may even con-

only became fully accepted in the 1980s. the microbial loop, which is function- tain some bacteria and archaea (Box 1). Permissionociety. is Allreserved. rights granted to in teaching copy this and research. for use article Republication, systemmatic ,

Their importance as photosynthetic pro- ally intertwined with the more familiar ’s ocean is most certainly a of ociety. S ducers of organic matter became evident of , , and car- microbes; without them it would be a end all correspondence to:Oceanography S [email protected] Th e or when so-called blue-green were nivores. It channels energy and carbon very different place, less hospitable to all acknowledged as being bacteria, and via bacteria to (Darwin’s infu- life. Indeed, without the activity of these the microscopic cyanobacterium of the soria), to larger such as , the cycles of would genus Synechococcus was discovered to and , and on to and very quickly come to a halt. This is not be abundant in the —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 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 , University About one-half of the in every bring it to a stop. of Georgia, Athens, GA, USA. Peter breath we take derives from photosyn-

J. leB. Williams is Professor Emeritus, thetic bacteria within the marine micro- MICROBIAL MD 20849-1931, U ociety, 1931, Rockville, Box PO 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 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- and fishes. biomass is too Box 1. The Kinds of Eukarya small even to show relative to others in Animals Figure 1. The entire , Fungi including protozoan microzooplankton, Plants Domain Archaea is typically some five to ten times the Domain Bacteria mass of all multicellular marine organ- Microorganisms isms (locally, these ratios vary widely). include members The potential metabolic dominance of of many branches of the 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 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 . Other fac- gens equal to 100 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 —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 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 Bacterivorous protozoans Fishes Organisms 1 Algal autotrophs rate s s

Bacterial autotrophs 0.1 Annual Production Bacterial 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 per unit weight by (1999), Pomeroy (2004), and Robinson and Williams (2005) microorganisms. Modified from Pomeroy (2001)

is a marine, rather than a , isolate. have been called the “ultimate swim- tent. Bacteria do not have a set period Although we usually consider num- ming stomachs” (Azam, 1998). Most of of quiescence, but just keep sampling bers and biomass as the significant the organic matter available to consum- their environment. When good times parameters of food webs, Figure 1 sug- ers in the ocean is used and respired by happen, resting cells rapidly enlarge and gests that surface area also provides bacteria (Robinson and Williams, 2005). mobilize enzymes. valuable insights. What is striking is the Many bacteria use flagellar to Because they are a large fraction of the overwhelming surface area associated locate and attach to organic particles biomass and, when active, have relatively with bacteria. If surface area is taken as where fast-growing cells digest all or high metabolic rates, microorganisms a for metabolism, this figure gives part of the , releasing dissolved dominate the flux of energy and bio- a simple illustration of the metabolic organic molecules into the water to be logically important chemical elements importance of bacteria in the oceans, utilized by the microbial in the ocean. Photosynthetic bacteria and it brings home the fact that the (Azam, 1998). often are the dominant producers of new oceans are a microbial world, not a Bacteria and archaea also are the organic matter in central ocean basins of fishes, dolphins, and whales. Enzymes ultimate survivors, living even in geo- (Figure 3). Archaea also extract energy bound to those living bacterial surfaces logically old rock formations (Lin et from reduced chemical compounds break down complex and even quite al., 2006). They possess a metabolic present in the water, such as , refractory organic materials—lignin, gearshift that only a few multicellular sulfide, or ammonium. For cellulose, chitin, and —into organisms, such as bears and humming- individual bacteria, their world consists, smaller, simpler molecules that can birds, possess. Unlike birds and beasts, more or less, of the cubic meter of sea- be absorbed and utilized by bacteria. bacteria alter not only their metabolic water in which they reside. Each cubic External digestive processes provide rate but also their morphology. Resting meter contains a diverse community of shared benefits for motile bacteria, which cells are small, with minimal water con- microbial residents and is visited peri-

30 Oceanography Vol. 20, No. 2 Mesozooplankton Figure 3. Simplified diagram of the Dissolved organic ocean’s food web showing the domi- matter nant roles of the microbial loop. The major fluxes of carbon and energy are delineated by continuous lines; fluxes Photosynthetic bacteria usually of lesser magnitude are delin- eated by broken lines. Mucus-net feed- Ciliates Fishes ers ( and other microphages) are separated from other mesozooplank- ton because of their different feeding Nanoflagellates mode. Other than the mesozooplank- ton (including mucus-net feeders) and Heterotrophic bacteria fishes (all blue boxes), the boxes rep- resent organisms that are a part of the microbial loop (green = photosynthetic and yellow = heterotrophic). Mucus-net feeders Archaea Particulate organic matter

odically by large swimming or falling consumed in turn by larger ciliated pro- ously does not change with size; it is organisms, fecal particles, and micro- tozoa. Ciliates are a staple food of cope- more about momentum or actually the scopic aggregates composed of all of the pods and other mesozooplankton that lack of it. A better analogy is the rapid organic and inorganic particulate mate- are the food of larval fishes (Figure 3). of movement of balloons rial in seawater. On the scale of micrometers, at which thrown in the air. A rapidly swimming many processes of the microbial loop bacterium will for a mere hydro- ROLES IN THE FOOD WEB occur, bacteria and protozoans are swim- gen bond length once it stops propelling Microorganisms are capable of creat- ming in water on a scale (so-called low itself—a deceleration force many times ing a sustained cycle of production and ) where the physics greater than driving a Formula I Grand decomposition of organic matter, requir- associated with movement is very differ- Prix racing car at full speed into a wall ing only the input of or the ent from that which we experience. It is of granite. Our intuitions, derived from chemicals released from and from hot vents that occur near undersea volca- nism. Phytoplankton and photosynthetic the total mass of bacteria in the ocean exceeds and chemosynthetic convert or bicarbonate the combined mass of zooplankton and fishes. and inorganic nitrogen and phosphorus into the organic constituents of their cells. Microflagellates eat heterotrophic often commented that on the microbial the scale we live in, serve us poorly when and the smaller autotrophic bacteria. scale, the system behaves as if the water thinking about the microbial world. In so doing, they usually control the had a viscosity of honey. The analogy is Traditionally, scientists viewed the numbers of bacteria in the sea, and are prone to be misleading as viscosity obvi- microbial food web as primarily a site

Oceanography June 2007 31 of remineralization, supplying nitrogen may fall slowly through that meter-sized the , of the system. We can- and phosphorus for use as nutrients by community. In passing, the particle accu- not sit and watch events as would the phytoplankton. Indeed, this is one of its mulates bacteria that attach, morph into ornithologist in the . Simulation important functions. However, assimila- larger cells, mobilize enzymes, and begin models have been helpful in bringing tion of inorganic elements into organic to digest the particle while multiplying together quantitatively the rate of fall matter by archaea and photosynthetic (2 times per day) in numbers (Azam et of fecal particles and aggregates, diffu- bacteria and its transfer via protozoans al., 1993). Some of the daughter cells sion rates of dissolved materials in the water, and swimming speeds of cope- pods and motile bacteria to achieve a Because they are a large fraction of the biomass and, virtual description of the natural his- when active, have relatively high metabolic rates, tory. Interactive work with comput- microorganisms dominate the flux of energy and ing simulations and experiments, often biologically important chemical elements in the ocean. aboard , that use a variety of chemi- cal and radioactive tracers, cell sort- ers, and has helped us to to metazoans is also significant, even may later depart the particle as it disin- refine our understanding of processes though the multiple transfers of organic tegrates (Jacobsen and Azam, 1984). The that occur on scales of less than a cubic matter that occur in blue-water food largest, heaviest fecal pellets fall into the centimeter in the ocean. However, our webs greatly reduce the efficiency of depths of the ocean before being utilized attempts to depict for this article the transfer to terminal consumers. In the as completely as possible by embed- distribution of bacteria and other organ- blue water, where most phytoplankton ded bacteria, but the majority, even in isms in a cartoon of a typical microli- are small and photosynthetic bacteria polar waters, disintegrate in the upper ter or nanoliter of water failed, because are often the dominant primary produc- 50–100 meters (LeFèvre et al., 1998). the space is 99.99999% water. This is ers of organic matter, only 1–2% of the not the rain forest. primary production may be assimilated MICROBIAL NATURAL HISTORY Bacteria and archaea are everywhere, finally by fishes (Ducklow et al., 1986). How do we know about bacterial and albeit with major differences in activ- That this food web supports fishes at all protozoan behavior that takes place on ity rates and lifestyles. Within these is a result of the versatility of the bacte- a in the sea? This is groups are many specialists with suites rial community in using many sources really natural history, a kind of observa- of enzymes for specific tasks. Much of nutrients and its rapid response tional investigation that has been done research has gone into understanding to new sources. relatively easily with birds and beasts the differences among polar, temper- Most of the time, in most of the for centuries. Describing the activities ate, and tropical regions, places of high ocean, bacteria in the active mode are of microorganisms in the ocean, on a versus low photosynthetic production, growing and dividing at a slow pace, microscopic scale, presents new chal- and between surface waters and abyssal circa 0.2 times per day, using often- lenges, however. On that scale (as on waters that are dark, relatively cold, and meager local sources of nutrients. others), the ocean is not completely or with sparse and patchy sources of nutri- Virtually fixed in place in the water, they continuously mixed. Just as there are tion. These microbial communities have await a helpful event. A passing zoo- microhabitats in a forest, nano- and persisted since the early history of the plankter may relieve itself, leaving a trail pico- occur in ocean water planet. A billion or more years ago, the of dissolved and particulate organic mat- (Azam, 1998). The natural history of microbial loop became a self-sustaining ter in the water. A ’s fecal pel- the microbial loop is still to some extent community of organisms. It now inter- let, or smaller microscopic particles that inferential, based on an understanding acts with the lesser mass of large, mul- have stuck together to form an aggregate, of the physics and chemistry, as well as ticellular organisms of the ocean in

32 Oceanography Vol. 20, No. 2 and phosphorus pass through the long, REFERENCES multistep microbial food web. Some of Azam, F. 1998. Microbial control of oceanic carbon flux: The plot thickens. Science 280:694–696. it is short-circuited by organisms called Azam, F., D.C. Smith, G.F. Steward, and Å. Hagström. microphages. They are salps, appen- 1993. Bacteria-organic matter coupling and its significance for oceanic carbon cycling. Microbial dicularians, and some plank- Ecology 28:167–179. ton, for example, krill, which are able Darwin, C. 1845. Journal of researches into the natural history and geology of the countries visited dur- to filter the protozoans and some of ing the voyage of H.M.S. Beagle round the world, the bacteria from the water. Salps and under the Command of Capt. Fitz Roy, RN. 2nd doliolids (prochordates) feed by pump- ed. John Murray, London. del Giorgio, P.A., and P.J. leB. Williams, eds. 2005. ing seawater through a fine mucus net Respiration in Aquatic Ecosystems. Oxford that they secrete and ingest, along with University Press, NY, 326 pp. Ducklow, H.W. 1999. The bacterial component of the bacteria, protozoans, and phytoplank- Figure 4. Mucus net of a with material behind oceanic euphotic zone. FEMS Microbiology Ecology 30:1–10. it that has been collected on the net. Dimensions ton caught on the net (Figure 4). Some Ducklow, H.W., D.A. Purdie, P.J. leB. Williams, and of the openings in the net are 0.2 x 2 micrometers, of the pterapods (planktonic mol- J.M. Davies. 1986. Bacterioplankton: A sink for permitting capture of microorganisms. Electron- lusks) cast mucus nets in the water to carbon in a coastal marine plankton community. micrograph by Shirley F. Nishino which microorganisms adhere. These Science 232:865–867. Jacobsen, T.R., and F. Azam. 1984. Role of bacteria in are the most direct and efficient paths copepod fecal pellet decomposition, colonization, for energy from microbes to larger growth rates and mineralization. Bulletin of Marine Science 35:492–502. significant ways, but the larger part of organisms (LeFèvre et al., 1998). Less- LeFèvre, J., L. Legendre, and R.B. Rivkin. 1998. Fluxes all energy captured by marine photo- efficient but more ubiquitous routes of biogenic carbon in the : roles of large microphagous zooplankton. Journal of synthesis, by both bacteria and plants, are through ciliates, the top Marine Systems 17:325–345. is consumed ultimately by microorgan- of the microbial loop, to copepods and Lin, L.-H., P.-L. Wang, D. Rumble, J. Lippmann-Pipke, isms (Ducklow et al., 1986; del Giorgio other mesozooplankton. In spite of the E. Boice, L.M. Pratt, B.S. Lollar, E.L. Brodie, T.C. Hazen, G.L. Andersen, and others. 2006. Long-term and Williams, 2005). Although the ocean length of the microbial , it is sustainability of a high-energy, low-density crustal contains a large volume of dissolved an important nutritional link in the sea, . Science 314:479–482. Pomeroy, L.R. 2001. Caught in the food web: organic matter too refractory for bacteria and there is a net balance of photosyn- Complexity made simple? Scientia Marina to process, some of it thousands of years thesis over respiration (Williams, 1998). 65(suppl. 2):31–40. Pomeroy, L.R. 2004. Building bridges across sub- old, it is an extremely small fraction That microbial food chain is of major disciplines in marine ecology. Scientia Marina of what has been produced over mil- significance in large parts of the ocean 69(suppl. 1):5–12. Robinson, C., and P.J. leB. Williams. 2005. Respiration and its measurement in surface marine waters. Pp. 147–180 in Respiration in Aquatic Ecosystems. P.A. del Giorgio and P.J. leB. Williams, eds, Oxford the natural history of the microbial loop is University Press, Oxford. still to some extent inferential, based on an Whitman, W.B., D.C. Coleman, and W.J. Wiebe. 1998. . The unseen majority. Proceedings understanding of the physics and chemistry, of the National Academy of Sciences of the United States of America 95:6,578–6,583. as well as the microbiology, of the system. Williams, P.J. leB., 1998. The balance of plankton res- piration and in the open ocean. Nature 394:55–57. Woese, C.R., and G.E. Fox. 1977. Phylogenetic lions of years. Microorganisms process where there is little production of the structure of the Prokaryotic domain: The pri- mary kingdoms. Proceedings of the National nearly everything, from a microscopic larger, nonbacterial phytoplankton, espe- Academy of Sciences of the United States of America aggregate of organic to a cially in the “clear blue water” in which 74:5,088–5,098. carcass on the bottom. Darwin suspected there might be life Not all energy, carbon, nitrogen, smaller than protozoa.

Oceanography June 2007 33