Review

The global ocean microbiome

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Science  11 Dec 2015:
Vol. 350, Issue 6266, aac8455
DOI: 10.1126/science.aac8455

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The ocean microbial system

The vast translucent oceans are teeming with microscopic life that drives significant life processes and elemental cycling on Earth. Yet how climate change will affect the functioning of this microbiome is not well understood. Moran reviews progress and the transformative discoveries made recently in marine microbiology that have led environmental, plant, animal, and even human microbiome research.

Science, this issue p. 10.1126/science.aac8455

Structured Abstract

BACKGROUND

Oceanographers began studying the ocean microbiome in earnest over four decades ago, when it was recognized that microbes are responsible for nearly all of the energy flux in this largest and most dilute biological system on Earth. Much has been learned about the microbes that play key roles in every marine element cycle, but much is still unknown about the factors regulating their activity. Although the number of marine microbes per liter of seawater reaches into the billions, their small size means that, statistically, each microbe is separated by 100 to 200 body lengths from its closest neighbors. Yet recognition of microscale structuring of both microbial communities and marine organic matter suggests that the ocean microbiome does not operate as stand-alone cells in a watery soup.

ADVANCES

Several decades of 16S ribosomal RNA gene analysis has revealed distinct and recurring bacterial communities in the ocean. More recent characterizations of marine archaea, protists, and viruses are filling out the taxonomic inventories of the ocean microbiome and showing that membership is predictable over seasons, ocean depth, and organic matter features. The retrieval of proteorhodopsin—a gene that allows cells to harvest energy from sunlight without complex photosynthetic machinery—from an uncultured ocean microbe marked the first exciting discovery from the use of “meta-omics” methodologies in the ocean. Now these techniques are the central tools for converting inventories of organisms and functions into explicit linkages between the two. Substantial progress has been made toward unraveling how and where microbes participate in ocean biogeochemical processes, as well as toward recognizing new categories of nonpredatory microbial alliances that operate based on the exchange of nitrogen, vitamins, hormones, and antibiotics.

Several characteristics of the ocean microbiome distinguish it from microbiomes on or in animals, plants, and soils. First, the primary producers that fuel the ocean are exclusively microbial and thus are a part of the microbiome. This is the case for photosynthesis in the surface ocean and for chemosynthesis carried out in deeper waters. The ocean microbiome is responsible for half of all primary production occurring on Earth. Second, trophic categories are particularly difficult to assign in the ocean microbiome, with no clear division of organisms into canonical autotrophic and heterotrophic roles. Proteorhodopsin, anoxygenic phototrophy, and chemolithotrophic energy acquisition from inorganic compounds create trophic mayhem among members of the ocean microbiome. Having multiple strategies for meeting metabolic requirements may be an advantage in this chemically dilute and physically dynamic environment. Last, heterogeneity in the structure of seawater organic matter has become a foundational concept for the ocean microbiome because it aligns with differences in microbial attributes. Bacteria and archaea that live singly in seawater differ from those that intermingle on the various marine polymer networks and organic surfaces in terms of phylogenetic affinity, metabolism, and capabilities for motility, chemotaxis, and defense. Single bacteria and archaea are numerically dominant in terms of cells, genes, and transcripts, but those clustered near surfaces have higher per-cell rates of metabolism and growth. The importance of material exchanges and signaling networks between neighboring cells in the ocean, as well as the consequences spatial arrangements impose on biogeochemical processing, are not yet understood.

OUTLOOK

Earth’s changing climate is predicted to decrease carbon fixation by microbial primary producers, favor smaller picophytoplankton over larger nano- and microphytoplankton, and impose stress on photosynthetic microbes that form calcium carbonate shells. The structure of phytoplankton communities, in turn, has implications for the abundance and composition of organic substrates for heterotrophic microbes, as well as for dictating which trophic strategies will be under selection in the future ocean. Taking stock of the ocean microbiome in terms of cells, genes, transcripts, and proteins now has a long tradition in oceanography. Linking these stocks with the regulation of critical ecosystem functions is the next challenge. One key step in this process is the identification of the molecules that pass between microbes as substrates, nutrients, signaling molecules, and defensive compounds; these are the “currencies” of ocean microbiome function.

Sampling the ocean microbiome.

(Left) New instruments such as the Environmental Sample Processor (ESP) (Monterey Bay Aquarium Research Institute) autonomously sample ocean microbes and environmental conditions while deployed at sea. (Right) Microbial cells preserved in metal pucks inside the ESP are removed for gene expression analysis.

PHOTOS: (LEFT) J. MOTARD-CÔTÉ; (RIGHT) A. BURNS

Abstract

The microbiome of the largest environment on Earth has been gradually revealing its secrets over four decades of study. Despite the dispersed nature of substrates and the transience of surfaces, marine microbes drive essential transformations in all global elemental cycles. Much has been learned about the microbes that carry out key biogeochemical processes, but there are still plenty of ambiguities about the factors important in regulating activity, including the role of microbial interactions. Identifying the molecular “currencies” exchanged within the microbial community will provide key information on microbiome function and its vulnerability to environmental change.

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