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Science 338, 628 (2012); DOI: 10.1126/Science.1208929

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Science 338, 628 (2012); DOI: 10.1126/Science.1208929 Marine Microbes See a Sea of Gradients Roman Stocker Science 338, 628 (2012); DOI: 10.1126/science.1208929 This copy is for your personal, non-commercial use only. If you wish to distribute this article to others, you can order high-quality copies for your colleagues, clients, or customers by clicking here. Permission to republish or repurpose articles or portions of articles can be obtained by following the guidelines here. The following resources related to this article are available online at www.sciencemag.org (this information is current as of November 1, 2012 ): Updated information and services, including high-resolution figures, can be found in the online version of this article at: on November 1, 2012 http://www.sciencemag.org/content/338/6107/628.full.html A list of selected additional articles on the Science Web sites related to this article can be found at: http://www.sciencemag.org/content/338/6107/628.full.html#related This article cites 48 articles, 21 of which can be accessed free: http://www.sciencemag.org/content/338/6107/628.full.html#ref-list-1 www.sciencemag.org Downloaded from Science (print ISSN 0036-8075; online ISSN 1095-9203) is published weekly, except the last week in December, by the American Association for the Advancement of Science, 1200 New York Avenue NW, Washington, DC 20005. Copyright 2012 by the American Association for the Advancement of Science; all rights reserved. The title Science is a registered trademark of AAAS. REVIEW tools and conceptual frameworks, if we are to understand the consequences of resource hetero- geneity and microbial behavior on diversity, pro- Marine Microbes See a ductivity, and biogeochemistry. How Heterogeneous Is the Ocean Sea of Gradients at the Microscale? Roman Stocker It has long been recognized that the water column is dotted with copious sources of microscale het- Marine bacteria influence Earth’senvironmentaldynamicsinfundamentalwaysbycontrolling erogeneity (Fig. 1). A ubiquitous case is the “phy- the biogeochemistry and productivity of the oceans. These large-scale consequences result from cosphere,” the region surrounding a phytoplankton the combined effect of countless interactions occurring at the level of the individual cells. At cell, which harbors gradients of dissolved organic these small scales, the ocean is surprisingly heterogeneous, and microbes experience an matter [DOM; operationally defined as the or- environment of pervasive and dynamic chemical and physical gradients. Many species actively ganic material <0.7 mminsize(2)] and oxygen exploit this heterogeneity, while others rely on gradient-independent adaptations. This is an that attract heterotrophic bacteria (4, 5). This exciting time to explore this frontier of oceanography, but understanding microbial behavior attraction can result in diverse ecological inter- and competition in the context of the water column’smicroarchitecturecallsfornewecological actions between bacteria and algae, from sym- frameworks, such as a microbial optimal foraging theory, to determine the relevant trade-offs biosis to parasitism, and can increase the fraction and global consequences of microbial life in a sea of gradients. of primary production used by bacteria (6). Equal- ly widespread are marine snow particles, aggre- wenty years ago much of microbial ocean- scale processes in the sea, including the cycling gates that also contain gradients of DOM and ography was based on the assumption that of most elements, the rates and fate of primary oxygen (7)andemanateintenseDOMplumesas Tmolecules and organisms are randomly production, and the generation of climatically they sink (8, 9). The particles and their plumes distributed, with little regard for gradients and active gases (2), yet they live and interact with the can attract and become growth hot spots for bac- behavioral responses (1). There is now abundant ocean at the microscale. In terms of relative scale, teria (9, 10). Strong gradients are further created evidence that nutrients are not homogeneously environmental conditions at tens of meters res- by excretions from larger organisms, cell lysis, and on November 1, 2012 distributed at the scales relevant to the microor- olution are to a microbe what the mean world sloppy feeding. These sources of heterogeneity, ganisms and instead frequently arise as microscale temperature is to an African lion: a useful metric along with a multitude of particle types ranging hot spots. Many bacteria exploit heterogeneity for global trends, but hardly a mechanistic eco- from colloids to fecal pellets to exopolymers, can by swimming toward the epicenter of hot spots, logical predictor. vary in size from micrometers to centimeters, and whereas others survive in low-concentration, uni- How large, then, is a microbial microenvi- harbor resource concentrations orders of magni- form background conditions. ronment in the ocean? Rather than being a fixed tude above background levels. Although tools to interrogate the behavior of volume (3), it depends on behavior and time, as These processes have led to the view that marine microbes at the level of single cells and simple calculations exemplify. For a nonmotile even a milliliter of seawater is far from homoge- their microenvironment have begun to be devel- bacterium (or archaeon), cell size (~0.4- to 2-mm neous (3). I suggest that microscale gradients are oped, the conceptual frameworks needed to eval- diameter) defines the microenvironment. For ex- in fact considerably more pervasive than even www.sciencemag.org uate the trade-offs and ecosystem implications of ample, nutrient uptake occurs from a small region these sources of heterogeneity indicate, for three life in microscale gradients lag behind. Integrat- surrounding the organism, the diffusion bounda- reasons. First, the majority of inputs of microbial ing microscale observationswithecologicalframe- ry layer, which spans a few cell diameters. There resources are heterogeneous at microbial scales: works will shed light on important unexplored is little motion of the cell relative to the sur- 10- to 1000-mmoildropletsoriginatingfromspills questions in microbial oceanography. What are rounding water, with Brownian diffusion allow- or natural seeps, 50- to 5000-mmgasbubbles the effects of gradients on microbial diversity ing a 0.4-mm–diameter cell to explore 45 pl of released from natural vents or injected by breaking in the ocean? How do they affect productivity? Do seawater (a ~35-mmcube)in10minand80nl waves, sediment grains resuspended by currents, Downloaded from the consequences of heterogeneity simply aver- (a ~430-mmcube)inaday. and dust particles of aeolian origin are all con- age out, justifying mean-field descriptions based In contrast, the microenvironment of a swim- stituents of large-scale events that for marine on bulk concentrations andaneglectofbehavior, ming bacterium is largely defined by its motility microorganisms resolve into a patchy landscape or do microscale gradients affect the rates and range. One can calculate that randomly swim- peppered with discrete resources and microscale fluxes of biogeochemical transformation? This ming at 50 mm/s enables a bacterium to experi- gradients. Review describes the nature and prevalence of ence 0.5 ml(a~0.8-mmcube)ofnewwaterevery Second, turbulence converts macroheteroge- microscale gradients in the ocean, the response 10 min and 0.8 ml (a ~1 cm cube) every day. neity into microheterogeneity. In the process of of microbes to these gradients, and the putative Chemotaxis (the ability to sense chemical gra- mixing a solute such as DOM, turbulent whirls mechanisms by which these processes can affect dients and direct motility accordingly) further in- stir the solute into ever-finer sheets and filaments the marine ecosystem at a global scale. creases the distance a microbe can traverse: a (see Box 1 and associated figure). This stretch- chemotactic velocity (the directional component ing and folding continues down to a scale below At What Scales Do Marine Microbes Interact of swimming) of 10 mm/s results in a net dis- which molecular diffusion dissipates gradients to with Their Environment? placement of 6 mm in 10 min. truly mix the solute. For typical marine turbulence To understand the behavior of an organism, it Microbial microenvironments can thus be large levels, this scale, known as the Batchelor scale, must be studied in relation to its immediate en- compared with cell size but are still tiny relative ranges from 30 to 300 mm. Thus, irrespective of vironment. Marine microorganisms affect large- to most oceanographic sampling methods. With the size of the DOM source, turbulence produces rare exceptions, these volumes remain difficult arichfabricofgradientsatthescaleofmicrobial to interrogate in situ, owing to the small size and microenvironments. Ralph M. Parsons Laboratory, Department of Civil and En- Third, chemical gradients are compounded by vironmental Engineering, 49-213, Massachusetts Institute of intermittency of microenvironments and the minus- Technology, 77 Massachusetts Avenue, Cambridge, MA 02139, cule amount of matter they contain. We must gain physical gradients. Microscale viscosity gradients USA. E-mail: [email protected] better access to the marine microscale, in terms of can develop inside and around particles, but also 628 2NOVEMBER2012 VOL338 SCIENCE www.sciencemag.org REVIEW in the bulk medium, where colloids and mucus chemotaxing into the DOM plumes emanating In contrast, copiotrophs are adapted to take sheets can form tangled polymer
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