PerspectiveOceanography

Microbes, Molecules, and Marine Ecosystems

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Science  12 Mar 2004:
Vol. 303, Issue 5664, pp. 1622-1624
DOI: 10.1126/science.1093892

Antonie van Leeuwenhoek (1632–1723), the first observer of bacteria, would be surprised that over 99% of microbes in the sea remained unseen until after Viking Lander (1976) set out to seek microbial life on Mars. Through much of the 19th and 20th centuries, microbiologists focused on life-threatening pathogenic microbes or microbes as models of how life “works” at the molecular level. But heightened concerns for ocean health and biodiversity, highlighted in the 2003 Pew Oceans Commissions report (1), prompted microbial explorations of the sea with state-of-the-art tools such as satellite and laser-based imaging, as well as massive genomic surveys rivaling the human genome project. This has led to a gold rush of discoveries underscoring critical influences of microbes on marine ecosystems and carrying significant implications for sustainability, global climate, and human health. The challenge is integrating these discoveries at the systems level to elucidate microbial roles in overall system resilience. Understanding the role of microbes in structuring healthy and stressed marine ecosystems will provide the mechanistic basis for prognostic models. Accomplishing this may require a new and unifying framework for conceptualizing these ecosystems.

Excitement over the “microbial ocean” was roused by the 1977 seminal discovery by Hobbie (2) and later studies that pelagic bacteria are hugely abundant (106 ml−1), accounting for most oceanic biomass and metabolism (3). They had eluded detection because most are extremely small—only a few percent of Escherichia coli in volume—and uncultivable. Thus, in order to measure bacterial biodiversity and in situ metabolism, microbial oceanographers had to devise cultivation-independent methods. Results show that bacteria are a major biological force in the oceanic carbon cycle and ecosystem structure.

Photosynthetic bacteria Prochlorococcus and Synechococcus are the most abundant oceanic primary producers, and their sequenced genomes provide new ecological insights (46). Other discoveries confront oceanographers and conservation biologists with the probability that many functional capabilities and mechanisms remain unknown. For instance, a bacterial gene for proteorhodopsin was discovered 3 years ago (7). This pigment, thought to exist only in Archaea, converts light energy directly into an electrical gradient across the cell membrane. The gene occurs in divergent marine bacterial taxa and diverse environments (8); hence, inclusion of proteorhodopsin activity may change oceanic energy budgets. Another important example is the discovery of oceanwide distribution of anoxygenic phototrophic bacteria that contribute to oceanic energy and carbon budgets (9). Nitrogen budgets, a regulating force of carbon processing and sequestration, must also be reconsidered given new evidence for microbial N2 fixation as a common feature of oceanic systems (10, 11). Despite tremendous diversity, a single bacterial clade can dominate numerically. The α-proteobacterial clade SAR11 constitutes ∼30% of Sargasso Sea surface cells (12), and a newly discovered cluster within the Roseobacter clade, found throughout temperate and polar regions, makes up ∼20% of Southern Ocean bacteria (13). Finally, massive marine prokaryotic metagenome sequencing is providing a tremendous database for discovering metabolic capabilities and new ways to conceptualize and study prokaryotic biodiversity (14).

Environmental genomics is also revealing bacterial interactions with marine animals, and their influences on animal populations and ecosystem function. Corals offer an excellent example. A recent study discovered 430 novel bacterial ribotypes associated with three coral species (15), and shifts in bacterial species composition appear to underlie coral health and disease (16, 17). Appreciating this diversity in conservation efforts is important because functional redundancy cannot be assumed.

Marine bacteria are but one microbial realm in the ocean for which discoveries with ecosystem consequences abound. Viruses were not studied until 1989 yet are the most abundant biological entities in the sea (107 ml−1). Bacteriophages induce bacterial mortality, creating a futile carbon cycle in which dissolved organic matter assimilated by bacteria is released via bacterial lysis and metabolized by other bacteria, enhancing upper-ocean respiration (18). Species specificity and host density-dependence lead phage to “kill the winner,” maintaining bacterial diversity, with implications for organic matter decomposition (19, 20). Phage diversity studies were initially restricted by the requirement for cultivated hosts. Now, cultivation-independent genomics reveal enormous diversity, including a picorna-like superfamily implicated in phytoplankton mortality, even of toxic bloom-forming algae (21, 22). Furthermore, specific cyanophage distributions vary from coastal to open ocean, likely influencing Prochlorococcus or Synechococcus host distributions differentially (23).

In view of microbial abundance, diversity, dynamics, and influence on ocean chemistry, ecosystem-based conservation models must explicitly include microbes, to develop a functional view that integrates microbes, macrobes, and abiotic ecosystem components. This requires going beyond biodiversity assessment, because functional diversity depends on the environmental context of microbial expression. The task concerns an age-old theme in ecology: scale, both spatial and temporal, and the integration of scales (see the figure). Microbes are no different from larger organisms in this sense—one must study them at habitat scales relevant to their adaptive strategies to determine how their metabolism influences larger-scale ecosystem dynamics. For microbes this spatial scale is miniscule, from micrometers to millimeters. Because microbes influence ecosystems through molecular interactions, for example, involving cell surface receptors, permeases, or enzymes, the scale reduces to macromolecular, or nanometers. Thus, microbes' ecosystem activities, whether they involve carbon cycling or pathogenesis toward marine animals, should be modeled as molecular events.

Microbes in marine ecosystems.

Highly abundant and diverse bacteria and viruses (green dots) interact with biotic and abiotic ecosystem components at the molecular, or nanometer, scale yet critically influence the functioning of complex, large-scale marine ecosystems [e.g. endangered coral reefs (right)]. An atomic force microscope image of marine polysaccharides (top), a biochemical pathways chart (background) and genome map of Prochlorococcus provide examples of the context for analysis of complex marine ecosystems as dynamic molecular architectures.

PHOTO CREDITS: (CORAL REEF) D. KLINE; (EPIFLUORESCENCE MICROGRAPH) J. FUHRMAN; (ATOMIC FORCE MICROGRAPH) V. SVETLICIC & E. BALNOIS; (BIOCHEMICAL PATHWAYS) BOEHRINGER MANNHEIM

Studies of biochemical interactions and fluxes have yielded valuable insights. The oceanic silicon cycle is being revised following the discovery that colonizing bacteria cause postmortem dissolution of silica from diatom cell walls (frustules). These bacteria secrete proteases that denude the silica shell of its protective protein layer and enhance silica dissolution rates (24, 25). Silicon cycling, in turn, regulates diatom productivity, which is important, for example, in carbon cycling and fisheries.

Genomics opens another dimension for integrating cell biochemistry and ecosystem dynamics. Genomic exploration of two Prochlorococcus ecotypes has not only identified features with “…obvious roles in the relative fitness of the ecotypes in response to key environmental variables…” but has also inferred biochemical bases for ecotype-specific environmental impacts (5). The Silicibacter pomeroyi genome is yielding ecophysiological insights into bacteria producing dimethyl sulfide (DMS), a volatile compound that influences cloud formation (26, 27). S. pomeroyi degrades dimethylsulfoniopropionate (DMSP) via several pathways, but only one leads to DMS; thus, the relative expression of particular DMSP-degrading enzymes regulates climate. Overarching the microbial activities is the physical organization of organic matter in seawater, allowing the visualization of ecosystems as molecular architectures. Seawater is structured with cross-linked polymers, colloids, and nano- and microgels, creating an organic matter continuum and a wealth of surfaces displaying activity and biodiversity hot-spots (3). This structure provides a spatial context for microbial interactions and adaptations, and permits ecosystem analysis in terms of molecular architecture and biochemical fluxes.

These discoveries illustrate that nanoscale biochemical bases of ecosystem function are tractable, informative, and indeed essential, if we are to develop mechanistic models of ocean-basin biogeochemical dynamics. Microbial oceanography has made remarkable strides toward system inventory, exposing tremendous diversity of microbial capabilities, and spatial and temporal dynamics. Although they reveal the incredible capacity of microbes to interact with ocean systems, these studies do not address system structure or organizational processes. Biosystems exhibit variability at all organizational scales, from gene expression to groups of diverse individuals, but all display molecular interconnectedness. Analysis of marine ecosystems as biochemical matrices is complex, but not unlike, for example, that of neurobiology and systems biology. Modeling efforts must incorporate interaction mechanisms and variability at all ecosystem scales, including the nanometer-to-millimeter realm of microbes and molecules. Such an analysis can now begin, but it will require a convergence of genomics and the nascent field of microscale biogeochemistry, addressing spatially explicit biochemical interactions and their ecosystem consequences. This approach will lead to new testable hypotheses and prognostic models.

We propose consideration of concepts that are driving systems biology with its goal of elucidating all significant molecular interactions underlying the structure and functioning of a cell or an organism. The approach can be extended to marine ecosystem analysis (“ecosystems biology”), in essence treating the ecosystem as dynamic molecular architecture and appreciating real-time expression as the mechanistic basis of ecosystem dynamics. Although the goal of treating organisms and the environment as a molecular continuum is huge, the rate of progress in genomics and proteomics and its integration into oceanography—a field rich in computational talent—promises success. Ecosystems biology offers a framework for integrating genomic, biochemical, and environmental data. This framework will also unify efforts for biodiversity conservation and conservation of desirable biogeochemical states of the ocean.

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