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Resourceful heterotrophs make the most of light in the coastal ocean

Key Points

  • Heterotrophic marine bacteria that live in surface waters use a range of strategies to obtain energy from sunlight, either directly or indirectly, even though they rely on organic compounds for most of their carbon needs. Studies of ecologically relevant cultured marine bacteria and metagenomic surveys have contributed significantly to a new understanding of these important ocean processes.

  • The absorption of sunlight by dissolved organic compounds in surface seawater results in the formation of carbon monoxide. Diverse marine bacterioplankton oxidize carbon monoxide for energy, which has implications for their cellular carbon budgets and the ocean–atmosphere flux of this greenhouse-relevant gas.

  • Bacteriochlorophyll a is found in surface-dwelling marine bacteria throughout the oceans and is used to generate energy from sunlight. Bacterioplankton that contain bacteriochlorophyll a probably do not fix carbon like oxygenic phototrophs, but instead use the energy to supplement a heterotrophic lifestyle. However, enhanced levels of anaplerotic carbon fixation have been proposed for some.

  • Proteorhodopsin proteins that are anchored in the membranes of marine bacterioplankton use sunlight to generate proton gradients. The remarkable abundance and broad taxonomic distribution of proteorhodopsin-encoding genes suggest that this is a major process by which ocean-surface bacteria obtain their energy.

  • As bacterioplankton do not produce carbon dioxide during the energy generation that is mediated by proteorhodopsin or bacteriochlorophyll a, these processes have implications for the marine carbon cycle.

Abstract

The carbon cycle in the coastal ocean is affected by how heterotrophic marine bacterioplankton obtain their energy. Although it was previously thought that these organisms relied on the organic carbon in seawater for all of their energy needs, several recent discoveries now suggest that pelagic bacteria can depart from a strictly heterotrophic lifestyle by obtaining energy through unconventional mechanisms that are linked to the penetration of sunlight into surface waters. These newly discovered mechanisms involve the harvesting of energy, either directly from light or indirectly from inorganic compounds that are formed when dissolved organic carbon absorbs light. In coastal systems, these mixed metabolic strategies have implications for how efficiently organic carbon is retained in the marine food web and how climatically important gases are exchanged between the ocean and the atmosphere.

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Figure 1: Light-linked bacterial and archaeal metabolisms in the coastal ocean environment.
Figure 2: Light-dependent processes at different ocean depths.
Figure 3: Light-supplemented bacterioplankton productivity in coastal communities.
Figure 4: Anaplerotic pathways for CO2 fixation.

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Acknowledgements

We are indebted to C. Fichot for modelling expertise, and thank S. Sun and E. Howard for bioinformatics assistance. Funding was provided by the Gordon and Betty Moore Foundation, the National Science Foundation, the National Oceanographic and Atmospheric Administration and the Office of Naval Research.

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Correspondence to Mary Ann Moran.

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DATABASES

Entrez genome

alphaproteobacterium HTCC2255

Silicibacter pomeroyi

Entrez genome Project

MED134

Entrez Protein

BchX

CoxL

proteorhodopsin

PufL

PufM

RecA

FURTHER INFORMATION

Mary Ann Moran's homepage

Glossary

Pelagic

Relating to or occurring in the water column.

Heterotrophic

The acquisition of metabolic energy by the consumption of living or dead organic matter.

Primary production

The original source of organic material in an ecosystem — plants, algae or chemosynthetic microorganisms.

Bacterioplankton

The bacteria that inhabit the water column of lakes and oceans, either freely suspended or attached to particles.

Biomass burning

The burning of living and dead vegetation, including the human-initiated burning of vegetation and natural, lightning-induced fires.

Km

The substrate concentration at which the reaction is half of the maximal rate.

Cultured representative

A member of a bacterial taxon that is capable of growth in the laboratory, typically reaching high densities on microbiological media.

Oligotrophic

An aquatic environment that has low levels of nutrients and algal photosynthetic production (for example, high mountain lakes or the open ocean).

Phototroph

An organism that derives energy from sunlight.

Autotrophic

An organism that synthesizes organic carbon from the fixation of inorganic carbon, for example, by photo- or chemosynthesis.

Anaplerotic mechanism

A cellular reaction that replaces intermediates of the citric acid cycle that have been siphoned off into biosynthetic pathways.

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Moran, M., Miller, W. Resourceful heterotrophs make the most of light in the coastal ocean. Nat Rev Microbiol 5, 792–800 (2007). https://doi.org/10.1038/nrmicro1746

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