This article has This been published in 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 portionthe ofwith any permitted articleonly photocopy by is machine, of this reposting, means or collective or other redistirbution A S E A O F M I cr O be S > SecTION IV. PROceSSES Oceanography > CHAPTer 8. ENerGY DISSIPATION, RESPIR ATION, AND GROWTH , Volume 20, , Volume Microbes and the Dissipation of Energy and Respiration: N umber 2, a quarterly journal of journal The umber 2, a quarterly From Cells to Ecosystems BY CR AIG A . CARLSON, PAUL A . deL GIORGIO, AND GerHArd J. HerNDL In the year 1974, Larry Pomeroy first chemistry is elucidated in studies of how In the contemporary aerobic ocean, O ceanography ceanography proposed that microbes were true mov- the flow of energy through microbial the metabolic strategy for the vast ers of energy and nutrients in marine processes manifests itself as demand for majority of prokaryotes is chemohet- S food webs (Pomeroy, 1974). This idea and recycling of elemental nutrients. erotrophy. Heterotrophic bacterio- ociety. Copyright 2007 by The 2007 by Copyright ociety. was later formalized as the “microbial Prokaryotes (bacteria and archaea) plankton are the major respirers (Sherr loop” (Azam et al., 1983; Pomeroy et al., are now recognized as the most abun- and Sherr, 1996; Rivkin and Legendre, this issue) in which energy and carbon dant living component of the biosphere 2001), with organic compounds serving lost from the planktonic food web in the with approximately 12 x 1028 cells found as both the electron donors as well as form of dissolved organic matter (DOM) in the oceanic water column (Whitman carbon sources, and oxygen functioning O ceanography ceanography O was recovered and repackaged by hetero- et al., 1998). This prokaryotic biomass as electron acceptor. As organic matter ceanography ceanography trophic bacterioplankton to particulate is comprised of vast phylogenetic diver- is catabolized, both organic matter and S ociety. ociety. organic matter (POM). Their ecological sity (Venter et al., 2004; Giovannoni O2 are consumed, resulting in anabo- S ociety. ociety. role within the microbial loop is to facili- and Stingl, 2005; Moran et al., this lism (biosynthesis) and CO production. A 2 ll rights reserved. Permission is granted to copy this article for use in teaching and research. Republication, systemmatic reproduction, reproduction, systemmatic Republication, article use for research. and this copy in teaching to granted ll rights reserved. is Permission S tate the transformation of DOM to POM issue; Edwards and Dinsdale, this issue, In terms of energy and carbon cycling end all correspondence to: [email protected] or Th e [email protected] to: all correspondence end (a trophic “link”) (Azam et al., 1983) or Breitbart et al., this issue) as well as within the ocean, it is these chemoor- to remineralize DOM back to its inor- metabolic diversity (King, 2005; DeLong ganotrophic organisms that are the most important physiological group. They are instrumental in the transformation of organic matter, its remineralization to Prokaryotes (bacteria and archaea) are inorganic constituents (Ducklow et al., now recognized as the most abundant O CRAIG A. CARLSON ([email protected]. ceanography ceanography living component of the biosphere... edu) is Associate Professor, Marine Science Institute, University of California, Santa S ociety, P ociety, Barbara, CA, USA. PAUL A. deL GIORGIO ganic constituents (a respiratory “sink”) et al., 2006). Although prokaryotic pro- is Associate Professor, Département O Box 1931, Rockville, MD 20849-1931, (Ducklow et al., 1986). These early stud- cesses and trophic interactions occur on des Sciences Biologiques, Université du ies laid the conceptual framework for the spatial scale of nanometers (Azam, Quebec à Montreal, Canada. GerHArd investigations that linked microbial pro- 1998), their sheer numbers and the J. HerNDL is Department Head, Biological cesses to the flow of energy in marine rates at which they operate have major Oceanography, Royal Netherlands food webs (microbial ecology or tropho- biogeochemical implications on the Institute for Sea Research (Royal NIOZ), dynamics). The link to ocean biogeo- scale of ecosystems. Texel, The Netherlands. USA . Oceanography June 2007 89 1986), and shaping of the organic and Substrate inorganic environment (Williams and I del Giorgio, 2005). These organisms and their associated processes will be the New cells focus of this article. II One of the fundamental proper- (biomass) ties that determines bacterioplankton’s ecological or biogeochemical role in the marine ecosystem is the amount of µ biomass produced per unit of organic a c1 C consumed, or the bacterial growth b efficiency (BGE) (Sherr and Sherr, c2 ATP 1996; del Giorgio and Cole, 1998). BGE c3 is a measure of the coupling between c4 d III catabolic (energy-yielding) reactions Products Cell or waste to anabolic (biosynthetic; energy- Storage requiring) reactions and is expressed by the formula, Figure 1. Substrate and energy flow within a cell. Substrate < 700 Da are actively taken up via membrane BGE = BP / (BP+BR) [1] proteins (I). As the substrate enters the cell via active uptake, it either enters into catabolic pathways (blue lines) or anabolic pathways (green lines). Monomers for anabolism can come preformed from the where BP is bacterial production and environment or as products of catabolism. The red-hashed lines represent the flow of energy to and from these metabolic pathways. Energy is conserved via substrate catabolism and ATP is produced at a rate a. BR is bacterial respiration. Here we As ATP is hydrolyzed, energy is released and utilized at rate b to drive anabolic processes such as produc- will examine how microbial energet- tion of new cells (growth; II) and production cell storage products (III). Energy is also utilized at various ics of heterotrophic bacteria partition rates to support processes that are independent of anabolism. This maintenance energy is used at rates c1 to activate uptake systems, c2 to fuel cell motility, c3 to actively eliminate waste, and c4 to repair cellular energy and carbon on a cellular level machinery. In the absence of exogenous organic substrates, the cell can yield ATP at rate d by catabolizing (Figure 1), how that partitioning affects storage material (endogenous substrates). Adapted from del Giorgio and Cole (1998) their growth efficiency, and how that growth efficiency affects their ecological and biochemical roles in the sea. et al., this issue, for details on these two through a membrane transport system CELLULAR BIOENerGETICS metabolic strategies), or the oxidation of to an electron acceptor. The generated The first law of thermodynamics states organic compounds (chemoorganotro- chemical energy is used to drive the cells’ that the total amount of energy in the phy). ATP is synthesized via one of three metabolic processes (Jones, 1983). universe is conserved and cannot be distinct mechanisms: substrate-level The second law of thermodynamics created nor destroyed. As a result, all phosphorylation (fermentation), pho- states that in all processes or reactions, organisms have evolved physiological tophosphorylation, or oxidative phos- some of the energy involved irreversibly strategies to conserve energy by col- phorylation (respiration). Except for loses its ability to do work as a system lecting, converting, and storing that obligate fermenters, all microbes carry moves from order to disorder (entropy). energy principally via the synthesis out respiration. On the cellular level, From the standpoint of energy flow of adenosine-5’-triphosphate (ATP). respiration is the key process of energy within a cell, the hydrolysis of ATP trans- Energy is harvested from light (photot- conservation in which an electrochemi- fers the energy conserved from catabolic rophy), the oxidation of inorganic com- cal potential is generated from the flow reactions to energy-requiring reactions pounds (chemolithotrophy) (see Kolber of electrons from reduced compounds that support anabolism (Figure 1). 90 Oceanography Vol. 20, No. 2 However, cells expend energy in ways polysaccharide capsule might act as Maintenance Metabolism that are independent of cell biomass pro- sorption/scavenging site for organic A more ecologically important mecha- duction via processes such as overflow molecules for subsequent cleavage by nism in natural systems is the free metabolism, futile cycles, and main- ectoenzymes and is constantly renewed energy allocated to nongrowth reac- tenance metabolism (see Russell and (Stoderegger and Herndl, 1998). Hence, tions. Known as maintenance energy, it Cook, 1995) (Figure 1). Thus, efficiency heterotrophic microbial processes might serves to keep entropy low by fixing what of energy use with regard to biomass be important sources of recalcitrant breaks within the cell; thus, it helps a cell production (growth efficiency) can vary DOM (Tanoue et al., 1995; McCarthy to maintain its molecular, cellular, and significantly depending on the physical- et al., 1998). The pool of recalcitrant or functional integrity (Hoehler, 2004). The chemical state of the environment. semi-labile DOM is biologically reactive. larger the partitioning of energy into However, its production and subsequent maintenance processes, the lower the Overflow Metabolism remineralization are uncoupled for time energetic efficiency of the cell.