271 13 Implications of Microbial Motility on Water Column Ecosystems Karen K. Christensen-Dalsgaard CONTENTS 13.1 Introduction 271 13.1.1 Microbial Ecology in a Larger Context 273 13.2 Generating Motion with Cilia or Flagella 275 13.2.1 Smooth Flagella 275 13.2.2 Hispid Flagella 276 13.2.3 Cilia 277 13.3 The Energetics of Motion 278 13.4 Feeding Mechanisms 282 13.4.1 The Coexistence of Filter Feeders 284 13.4.2 Attaching to Particles while Feeding 288 13.5 Orientation to Stimuli 290 Acknowledgments 293 References 293 13.1 INTRODUCTION All aquatic bodies in the world, from the smallest forest ponds to the open ocean, house complex and diverse microbial ecosystems. When it comes to things such as number of species and carbon and nutrient turnover, unicellular organisms com- pletely dominate many aquatic ecosystems, and organisms on the size scale of fish are only minor players, contributing little to the overall balance. In environments dominated by open water, such as marine systems and those of large lakes, most of the photosynthetic activity is carried out by microscopic phytoplankton cells. In many ways, the microbial biota is as fascinating and complex as the apparently more flashy systems of tropical forests or coastal marine macroscopic ecosystems. Pelagic microbial biota differ from systems of larger organisms in many respects. At the microbial level, aquatic systems are highly heterogeneous, and microorgan- isms live in and are adapted to a world of alternating feasts and famines [1]. This requires an ability to survive the famines as well as an ability to move in response 3209_C013.fm Page 271 Thursday, November 10, 2005 10:49 AM Copyright © 2006 Taylor & Francis Group, LLC 272 Ecology and Biomechanics to chemical gradients, which the microorganisms cannot perceive over the length of their bodies, in order to utilize the patchy resources. Microorganisms function at very low Reynolds numbers and thus in an environment entirely dominated by viscous forces; typically, microorganisms are too small to have sensory organs with which they can perceive prey unless they make contact with them. This leaves them only a few possible means of locomotion and feeding. Nevertheless, a large and diverse range of morphologies has developed (Figure 13.1), and numerous species FIGURE 13.1 The diversity of the microbes represented by four genera, not drawn to scale. (A) Diaphanoeca , a flagellate with a smooth flagellum and a “cage” around the cell that increases the drag on the organism and thus the filtration efficiency (see Section 13.4.2). (B) Paraphysomonas , a flagellate with one short, smooth flagellum, one hispid flagellum (see Section 13.2), and a cell body covered by silica spikes. (C) The ciliate Tintinnidium incorpo- rates agglutinated material into its lorica and has most of its cilia confined to its anterior end. (D) Pleuronema has a cell body entirely covered by cilia. 3209_C013.fm Page 272 Thursday, November 10, 2005 10:49 AM Copyright © 2006 Taylor & Francis Group, LLC Implications of Microbial Motility on Water Column Ecosystems 273 that occupy apparently similar niches coexist. As in other ecosystems, the peculiar characteristics of microbial ecosystems are nothing but a sum of the characteristics of each of the individual organisms of which it is composed and their response to the prevailing environment. Unlike systems of larger organisms, however, the micro- bial biota benefits from an absence of complex behavioral responses. Because of this, the characteristics of these ecosystems can in principle be understood directly from the mechanics and physiology of the individual organisms and their (to a large extent) predictable responses to stimuli. In this chapter, I review some aspects of the existing knowledge on this topic and present some new calculations. I focus on pelagic systems and organisms that swim by cilia and flagella, which is the case for almost all motile pelagic microbes. I do not consider factors affecting the photosynthetic rate of autotrophic protozoa but deal only with the heterotrophic aspects of the microbial ecosystem. Unlike larger organisms, the distinction between autotrophic and heterotrophic in the micro- bial world is not clear. Many heterotrophic flagellates also contain chloroplasts [2]; even within the same species, there may be individuals with or without chloroplasts. However, because autotrophic flagellates are capable of ingesting particles at rates similar to those of apochlorotic flagellates [2,3], in this review they are grouped together with the rest of the heterotrophic flagellates. 13.1.1 M ICROBIAL E COLOGY IN A L ARGER C ONTEXT It is well known that the classical textbook food chain of phytoplankton being eaten by copepods being eaten by fish and so forth is a huge oversimplification and describes at best only a minor part of the aquatic food chain [4]. Depending on conditions, 1 to 60% of the phytoplankton primary production is lost immediately as dissolved organic matter (DOM), probably mainly through lysing of phytoplank- ton cells [5–7]. Because of their small size and thus high surface to volume ratio, bacteria are highly efficient in the uptake of DOM [8], and the bacterial production based on phytoplankton exudates can be as much as 18 to 45% of the primary production. Heterotrophic protozoa such as flagellates and ciliates are efficient grazers on bacteria and other small particles. Through their large numbers and high volume specific grazing rates, they are capable of clearing 3 to 100% of the entire water column for small particles per day. The average values lie between 7 and 90%, depending on the area studied [9–12]. Much of the grazing seems to be carried out by minute eukaryotic organisms not much larger than bacteria [13]; this, however, varies. Flagellates are generally shown to be the most important grazers on bacteria; ciliates, like flagellates, mainly graze on larger particles, but ciliates can also be important bacteriovors [12]. The importance of heterotrophic microorganisms in the ocean seems to vary with the season; they may mainly be important after the spring bloom under summer stratification when the phytoplankton is dominated by small forms [11]. Bacterial numbers remain fairly constant over time in marine systems, being typically around 0.5 to 3 × 10 6 ml 1 ; fluctuations in nutrient and DOM avail- ability are apparent instead in fluctuations in the numbers of bacterivorous protozoa. 3209_C013.fm Page 273 Thursday, November 10, 2005 10:49 AM Copyright © 2006 Taylor & Francis Group, LLC 274 Ecology and Biomechanics Thus, the bacterial communities seem top-down controlled by grazing rather than limited by nutrients [4,9,10,13]. Flagellates may, for example, be consumed by ciliates that are in turn consumed by larger organisms such as copepods. Thus, the carbon originally lost as DOM is returned rather inefficiently to the traditional food chain through what has been denoted the microbial loop (Figure 13.2) [4]. In this way, protozoa form an important link from the DOM to higher organisms. They do not, however, specifically prey on bacteria but instead ingest particles in the right size class, and many flagellates are capable of ingesting particles their own size or in a few cases even larger, (e.g., see Refs. [14,15]). Small phytoplankton cells as well as other protozoa may be ingested as efficiently as, or even more efficiently, than bacteria [14,16–18]. Thus, protozoa may also function as sinks removing carbon from the system through increasing the number of trophic levels and so respiratory costs (Figure 13.2). Whether protozoa function mainly as sinks or links depends on the relative abundance of bacteria and small phytoplankton. FIGURE 13.2 A much simplified version of the pelagic ecosystem. Black solid arrows indicate the classical food chain. Open arrows with a solid line represent the microbial loop functioning as a link that returns DOM to the higher trophic levels. Gray arrows show how the microbial loop can function also as a sink, which results in a higher number of trophic levels and thus higher respiratory costs. Open arrows with dotted lines show ingestion by heterotrophic phytoplankton. Zooplankton Phytoplankton Bacterioplankton DOM Heterotrophic flagellates Ciliates 3209_C013.fm Page 274 Thursday, November 10, 2005 10:49 AM Copyright © 2006 Taylor & Francis Group, LLC Implications of Microbial Motility on Water Column Ecosystems 275 13.2 GENERATING MOTION WITH CILIA OR FLAGELLA Microorganisms operate at Reynolds numbers (Re) << 1, and so in a world where all fluid motions are reversible, they are excluded from any form of propulsion that makes use of the inertia of the water. Octopuses or jellyfish shrunk to the size of protozoa and trying to move would simply be moving back and forth on one spot. In order to move, microorganisms instead make use of the difference in drag of a cylinder moving perpendicular compared to parallel to the flow; the resistance to normal motions of a cylinder is somewhat higher than the resistance to tangential motions. This is the principle behind motion by smooth and hispid flagella as well as cilia. Because of the insignificance of inertial effects at low Re, the motion of an object is only possible as long as a force acts upon it. If one attempted at low Re to throw a ball, it would never leave the hand (see, e.g., Ref. [19]). 13.2.1 S MOOTH F LAGELLA Because of the differences in drag, a moving cylinder tilted toward the direction of motion will exert a force on the fluid normal to the length of the cylinder (Figure 13.3). This is the principle behind flagellar propulsion first noted by Taylor [20,21]. Thus, contrary to appearance, the mechanics of flagellar motion is more closely related to that of a snake moving through sand than that of eels or water snakes swimming. Motion is generated by the propagation of planar or three-dimensional helical waves along the length of the flagellum. This generates a force normal to the segments of the flagellum that are tilted to the direction of the wave propagation (Figure 13.3). The propulsive effect depends on this force exceeding the retarding components of tangential forces acting along the body [22–24]. FIGURE 13.3 The generation of motion with smooth (upper) or hispid (lower) flagella. The black arrows represent propulsive force or thrust, the gray arrow shows the direction of flagellar wave propagation, and the white arrows indicate the overall direction of the resulting fluid motion with respect to the cell. 3209_C013.fm Page 275 Thursday, November 10, 2005 10:49 AM Copyright © 2006 Taylor & Francis Group, LLC 276 Ecology and Biomechanics The fluid dynamics of bacterial and eukaryotic flagella are similar, but they differ in all other respects. Eukaryote cilia and flagella are around 0.2 μm in diameter and composed of the well-known 9 + 2 structure of inflexible microtubules that slide relative to each other. The bacterial flagellum is about 0.02 μm in diameter and is in itself completely immobile. It is composed of molecules of the protein flagellin that form a hollow tube. Perhaps unique in the biological world, the bacterial flagellum rotates continuously around its own axis [25] because of two rings that rotate relative to each other [26–28]. In this way, helical waves are propagated along the flagellum. Bacteria often have many flagella, which tend to form a bundle or bundles because beating filaments in the vicinity of each other tend to be synchro- nized through viscous coupling [20,29]. The flagella of this bundle are only separated during tumbles (see Section 13.5). Both helical and planer waveforms have energetic disadvantages. In planar waves, the segments of the flagellum nearly parallel to the wave direction produce only drag and no thrust [30]. All segments of the helical waves produce thrust but also generate a torque on the organism that must be counterbalanced by the counter- rotation of the cell body. This reduces the swimming speed proportionally to the effective rotation rate [31]. It has been proposed that the body movements of micro- organisms rotated around their axis could contribute to the thrust in the manner of a rotating inclined plane [32,33], but this contribution would in most cases be negligible [34]. One interesting exception is the bacterium Spirillum , which has a spiral-shaped body. It uses the flagella to generate a rotation of the cell body, which then moves through the fluid much in the manner of a corkscrew through a cork [35–37]. 13.2.2 H ISPID F LAGELLA Hispid flagella have rigid hairs, or mastigonemes, protruding from the flagellum (Figures 13.1B and 13.3). They are curious in that they pull the cell body in the same direction as that of the wave propagation, opposite to that of smooth flagella. This is because the movement of the individual mastigonemes produces thrust in the direction of the cell body (Figure 13.3), and given sufficiently large numbers of mastigonemes, it is predominantly these, and not the flagellum itself, that moves the fluid [38,39]. The number and characteristics of the mastigonemes required may depend on the relative amplitude and wavelength of the flagellum [38,40,41]. The- oretically, only relatively inflexible mastigomenes should be capable of moving the fluid [39,42]. Dinoflagellates, however, have mastigonemes that appear flexible, and yet they always rotate counterclockwise in the direction of the flagellar beat of the transverse flagellum [43]. Thus, it seems that our understanding of the functioning of mastigonemes is not yet complete. Flagellates with hispid flagella are common in all aquatic habitats, and this type of flagellum is present in a number of unrelated families. Because the presence of mastigonemes is not a primary character, it must provide important competitive advantages in microbial ecosystems. The importance of mastigonemes in evolution and ecology is, however, as yet poorly understood. They could improve the swim- ming efficiency of the cells, because the previously described energetic 3209_C013.fm Page 276 Thursday, November 10, 2005 10:49 AM Copyright © 2006 Taylor & Francis Group, LLC Implications of Microbial Motility on Water Column Ecosystems 277 disadvantages of smooth flagella are not present in hispid flagella. The flagellum itself, however, will work against the motion of the fluid, so the picture is not clear. Another possibility is that the mastigonemes can function as mechanoreceptors or in feeding because the anterior position of the hispid flagellum would make it well placed to work also as a sensory or food-intercepting organelle. The mastigonemes also make it possible for hispid flagella to move fluid across or even perpendicular to the flagellar axis, something that is not possible for smooth flagella [44]. It has already been shown that Paraphysomonas uses its flagellum for intercepting prey and increases its effective feeding area by utilizing this possibility [44]. This, how- ever, may be a special case. 13.2.3 C ILIA Cilia make direct use of the differences in drag between cylinders moving normal compared to tangential to the fluid in generating motion. The movement of the cilia consists of a power stroke in which the cilia forms a cylinder with a motion normal to the fluid, and a recovery stroke where most of the cilia moves tangentially with respect to the fluid (Figure 13.4). Whereas flagellates typically have only one or few flagella, ciliates must have thousands of cilia to produce motion. They are typically arranged in rows in which the cilia beat in metachronical waves, i.e., waves formed by a slight phase lag between adjacent cilia. These waves seem to be fluid dynamical in origin because they can be explained largely through the viscous coupling of adjacent cilia [45,46]. Another important aspect of the functioning of the cilia is the proximity of the cell wall. During the power stroke, when the cilium is extended away from the cell wall, it is capable of carrying along with it a large envelope of fluid. During the recovery stroke, the cilium moves close to the surface of the cell, and because of the viscous interactions with the wall, the cilium cannot carry as much fluid with it. Hence, there is a net movement of fluid down the surface of the cell, which contributes to the motion of the organism [47]. The fact that the ciliates move by moving fluid over the cell surface results in a much steeper velocity gradient over the surface than that found in inert bodies being pulled through the fluid by an external force, such as sedimenting organisms. Bodies pulled in this way carry more fluid along with them, and so they disturb the fluid much more than swimming cells [47,48]. Because predators may perceive prey through fluid dynamic signals such as shear [49,50], this reduces the visibility of the ciliates. FIGURE 13.4 Movement of a cilium. The movement from position 1 to 3 constitutes the power stroke and from 3 over to 4 and 5 and back to 1 constitutes the recovery stroke. Movement purely related to the recovery stroke is drawn with dashed lines. 5 1 2 4 3 3209_C013.fm Page 277 Thursday, November 10, 2005 10:49 AM Copyright © 2006 Taylor & Francis Group, LLC 278 Ecology and Biomechanics Flagellates, which pull an inert cell body through the fluid with a flagellum, do not have this advantage, but they are also typically smaller and slower. Hence, it is not clear under which conditions flagellates are hydrodynamically more visible than ciliates. Ciliates that have the cell body only partially, as compared to fully, covered by cilia could also generate a larger scale flow field around the cell body. Thus, it seems that the exact mechanism by which protozoa generate motion influences their relative visibility toward different types of predators and so influences their relative predation rates. Though this has important ecological implications, there have to my knowledge not been any thorough investigations of this phenomenon on protozoa. Only work on how foraging behaviors influence hydrodynamic visibility in copepods [51] and on how size and velocity of an assumed nonciliated particle affects its visibility [49] have been carried out so far. 13.3 THE ENERGETICS OF MOTION One of the curious aspects of microbial ecosystems compared to those of larger motile organisms is the apparent lack of an optimal swimming speed. It has often been stated that the energy spent by microorganisms on swimming constitutes only a minute part of their metabolism (e.g., Refs. [52,53]). In light of this, it should always be advantageous for microorganisms to swim as fast as possible because increasing their swimming speed will increase the contact rate with prey and thus the feeding rate. In spite of this, there are large differences in swimming speed between different species within the same size class and feeding on the same prey. The extent of this cannot be explained by differences in drag of the feeding appa- ratuses, as even within species that do not have retractable feeding structures, large variations in swimming velocity occur [54]. This variation should provide a firm basis for natural selection toward higher swimming speeds. So why do many micro- organisms still swim relatively slowly? One answer could be to reduce the probability of being preyed upon themselves. Contact rates between predator and prey are dependent not only on the swimming speed of the predator, but also on the swimming speed of the prey [55]. However, flagellates often seem bottom–up rather than top–down regulated (e.g., for instance Refs. [10,56]). Furthermore motility, while increasing the contact rate, may decrease the interception rate, hence in reality potentially providing protection from predation [57]. Thus, this does not seem to be satisfactory as the only answer. In most previous studies, only the drag on the cell body itself was used in the energy budget calculations. The drag on the cell body, however, constitutes only a minute part of the overall energy expenditure of motion; most of the energy is used in overcoming the tangential drag on the flagellum [22,30,31,39,58]. The total power consumption by a flagellum propelling a microorganism by helical motions is given by [31]: (13.1) PrU= − ηπμ 12 6 3209_C013.fm Page 278 Thursday, November 10, 2005 10:49 AM Copyright © 2006 Taylor & Francis Group, LLC Implications of Microbial Motility on Water Column Ecosystems 279 where P (J s –1 ) is the average power consumption, r (m) is the radius of the organism, μ (N s m –2 ) is the viscosity of water, and U (m s –1 ) is the swimming speed of the organism. η –1 is a nondimensional parameter defining the swimming efficiency of the organism. The optimal (smallest possible) value of η –1 that is achievable for a given organism depends on factors such as relative size of the cell body and relative length and width of the flagellum. The larger the cell body or the thicker the flagellum compared to its length ( L ), the less the possible efficiency. Whereas an organism with L / r = 10 and r = 50 × the radius of the flagellum can, in principle, achieve an optimal η –1 of 125, an organism with the same radius of the flagellum but L / r = 5 will not be able to do better than a η –1 of 210. The actual value of η –1 for a given organism can in principle range from this optimum to infinity, depending on flagellar parameters such as amplitude and frequency [31]. The value will only approach infinity if, for instance, the amplitude of the flagellum is going toward zero, resulting in very inefficient swimming. I will assume that the flagellates are swimming at constant speed until they encounter a food particle, then stop their motion for the time it takes to ingest the food particle, and then immediately reassume constant forward motion, as is seen for, e.g., Paraphysomonas vestita . The ingestion rate over time can then be calculated to be: (13.2) where I (particles s –1 ) is the ingestion rate, C (particles m –3 ) is the concentration of food particles, V (m 3 s –1 ) is the volume of liquid that passes through the area swept for particles over time ( V = UA , where A is the area swept for particles), and i (s particle –1 ) is the time it takes for the protozoon to ingest one food particle. I have assumed the following: The bacteria have a radius of 0.3 μm and are similar to E. coli with 26% of their volume composed of organic compounds, of which 8% is lipids and 92% is other organic compounds [59]. The energetic value of lipids is taken to be 37 KJ g 1 , and the energetic value of other compounds is taken to be 17 KJ g 1 . The bacteria do not swim. The protozoa have a radius of 3 μm, and the flagellum has a length of 30 μm and a radius of 0.1 μm. At these values, the energetic optimum of the organism lies at approximately η –1 = 150. The protozoa are assumed not to spend any energy on motion while in the process of ingesting a particle, and when swimming, do so close to their energetic optimum. They can ingest 60% of their volume per hour in accordance with the data in, e.g., Ref. [52], giving an average ingestion time of 6 sec. Ingested carbon not used in respiration for the purpose of motion is used in growth, with a growth efficiency of 40%. In this case, A is assumed to be equal to the transectional area of the body of the protozoa, as is seen in P. vestita [54]. From these assumptions, I have calculated the growth rate of the protozoa as a function of swimming velocity at different bacterial concentrations (Figure 13.5A and 13.5B). How the growth rate varies with swimming speed depends greatly on the con- centration of food particles. At concentrations of 10 11 particles m –3 , the growth rate I CV i = + − 1 1 () 3209_C013.fm Page 279 Thursday, November 10, 2005 10:49 AM Copyright © 2006 Taylor & Francis Group, LLC 280 Ecology and Biomechanics is effectively zero until the velocity is 180 μm sec –1 , with a small optimum of 1.85 × 10 –4 hr –1 at 91 μm sec –1 . At velocities above 180 μm sec –1 , the growth rate becomes increasingly negative. At 10 12 particles m –3 , the growth rate increases to a maximum of 1.61 × 10 –2 at a velocity of 850 μm sec –1 , then decreases again. At higher particle concentrations than this, the growth rate increases continuously with velocity for realistic values of potential swimming speed. The value however reaches an asymptotic value toward the maximum growth rate and so, after the asymptotic level is reached, a further increase in swimming speed does not significantly increase growth rates. The growth rates found are well in accordance with previous values obtained experimentally of growth rates for the given particle concentration (e.g., Refs. [52,60]. FIGURE 13.5 Theoretical growth rate of protozoa as function of their swimming speed at bacterial concentrations of (A ) 10 11 and 10 12 bacteria per cubic meter and (B) 10 13 to 10 15 bacteria per cubic meter. 0.02 0.01 10 12 m –3 10 11 m –3 0 0.015 0.005 –0.005 Growth rate hour –1 –0.015 –0.01 –0.02 0 100 200 300 Swimming speed, µm s –1 (a) 400 500 600 700 800 900 1000 0.25 0.2 0.15 Growth rate hour –1 0.05 0 0 100 200 300 Swimming speed, µm s –1 10 15 m –3 10 14 m –3 10 13 m –3 (b) 400 500 600 700 800 900 1000 0.1 3209_C013.fm Page 280 Thursday, November 10, 2005 10:49 AM Copyright © 2006 Taylor & Francis Group, LLC [...]... rotation and mechanism of bacterial motility, Nature, 249, 73, 1974 26 Depamphilis, M.L and Adler, J., Fine structure and isolation of hook-basal body complex of flagella from Escherichia-coli and Bacillus-subtilis, J Bacteriol., 105, 384, 1971 27 Okrend, A.G and Doetsch, R.N., Plasmolysis and bacterial motility — a method for study of membrane function, Archiv Mikrobiol., 69, 69, 1969 28 Vaituzis, Z and. .. 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Flagella 275 13. 2.1 Smooth Flagella 275 13. 2.2 Hispid Flagella 276 13. 2.3 Cilia 277 13. 3 The Energetics of Motion 278 13. 4 Feeding Mechanisms 282 13. 4.1 The Coexistence of Filter Feeders 284 13. 4.2. 13 Implications of Microbial Motility on Water Column Ecosystems Karen K. Christensen-Dalsgaard CONTENTS 13. 1 Introduction 271 13. 1.1 Microbial Ecology in a Larger Context 273 13. 2. few possible means of locomotion and feeding. Nevertheless, a large and diverse range of morphologies has developed (Figure 13. 1), and numerous species FIGURE 13. 1 The diversity of the microbes