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Microbial oceanography and the Hawaii Ocean Time-series programme

Nature Reviews Microbiology volume 12, pages 699–713 (2014)Cite this article

Subjects

Key Points

  • Marine habitats and the ecosystems that they support are diverse, complex and grossly undersampled, despite their importance to global processes and planetary habitability.

  • Microbially mediated biogeochemical cycles and metabolism are time-variable, climate-sensitive, non-steady-state processes and must be studied as such.

  • Microbial community structure, gene regulation and population interactions are dynamic features of marine ecosystems with substantial variation on multiple time scales, ranging from diel to decadal, and beyond.

  • Long-term (>1 decade), time series observations of microbial and biogeochemical processes provide invaluable data on genetic diversity and evolution, as well as the environmental controls on fundamental fluxes of energy and matter.

  • The establishment of long-term microbial observatories, including programmes like the Hawaii Ocean Time-series (HOT) provide platforms for collaborative research, support the conduct of transdisciplinary hypothesis-testing field experiments, and function as loci for the education and training of the next generation of leaders.

  • The relatively new discipline of microbial oceanography represents enormous opportunity to develop a more comprehensive understanding of the impacts of humans on microbial processes in the sea.

Abstract

The Hawaii Ocean Time-series (HOT) programme has been tracking microbial and biogeochemical processes in the North Pacific Subtropical Gyre since October 1988. The near-monthly time series observations have revealed previously undocumented phenomena within a temporally dynamic ecosystem that is vulnerable to climate change. Novel microorganisms, genes and unexpected metabolic pathways have been discovered and are being integrated into our evolving ecological paradigms. Continued research, including higher-frequency observations and at-sea experimentation, will help to provide a comprehensive scientific understanding of microbial processes in the largest biome on Earth.

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Figure 1: Station ALOHA habitat characteristics.
Figure 2: Selected examples of temporal variability in the NPSG.
Figure 3: Prochlorococcus spp. distributions and dynamics.
Figure 4: Temporal and depth variability in primary production at Station ALOHA.

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Acknowledgements

The authors acknowledge the US National Science Foundation (NSF) for sustained support of the Hawaii Ocean Time-series (HOT) programme (including the current grant OCE1260164). In addition, funding from the NSF to the Center for Microbial Oceanography: Research and Education (C-MORE) (grant EF0424599), the Gordon and Betty Moore Foundation (Marine Microbiology Investigator #3794), the Agouron Institute and the Simons Foundation to the Simons Collaboration on Ocean Processes and Ecology (SCOPE) support research at Station ALOHA (A Long-term Oligotrophic Habitat Assessment). They also acknowledge the dedicated efforts of the HOT team, including researchers, students, postdoctoral researchers and staff, who have all made important contributions to the HOT programme.

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  1. Daniel K. Inouye Center for Microbial Oceanography: Research and Education, University of Hawaii, 1950 East-West Road, Honolulu, 96822, Hawaii, USA

    David M. Karl & Matthew J. Church

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Correspondence to David M. Karl.

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Glossary

Gyres

The vast ecosystems that encompass open ocean waters of the tropical and subtropical regions of the oceans. The circular movements of the gyres, deriving from the combination of wind stress on the sea surface and the rotation of the Earth, result in physically isolated, stratified upper ocean waters that are persistently devoid of bioessential inorganic nutrients.

Biome

Contiguous habitats that share similar biogeochemical and physical properties.

Oligotrophic

A term used to describe environments that are characterized by low concentrations of growth-requiring nutrients and, consequently, low microbial biomass. Such habitats dominate the upper ocean of the large subtropical gyres. An oligotroph is the term used to describe an organism that is adapted to growing in habitats with low-nutrient conditions.

Euphotic zone

The region of the well-lit upper ocean that sustains the net production of organic matter. Often defined by the depth of penetration of sunlight, typically the depth to which 0.1 % of the light intensity that is observed at the surface ocean penetrates. In clear, open ocean ecosystems, the euphotic zone can extend to 150–200 m.

Climatology

In oceanography, this term refers to the determination of the mean ecosystem state, which requires averaging of time-resolved observations of sufficient duration to adequately sample processes underlying the dominant modes of ecosystem variability.

Primary production

The synthesis of organic matter from inorganic carbon. In the ocean, the vast majority of primary production is fuelled by photosynthesis.

Mesoscale eddies and Rossby waves

Physical processes that occur at spatial scales of 50–500 km and generally persist for 10–100 days. Such processes can originate from instability in the flow of currents owing to topographic features, variations in wind stress at the surface of the ocean or result from shear in the flow of waters of differing physical properties (that is, viscosity and density), such as along frontal boundaries. Such physical perturbations can propagate energy through the ocean in the form of waves or can result in the formation of isolated circulation vortices (similar to a cyclone in the atmosphere) that horizontally transport water of similar physical properties.

Biogeochemistry

The study of the interactions between biological processes and geochemical properties on Earth.

Phycobiliproteins

Proteins that are found in the photosynthetic light-harvesting complexes of various phototrophic cyanobacteria and eukaryotic algae. The proteins capture light energy and, via fluorescence events, transfer energy to photosynthetic reaction centres.

Genetic microadaptation

Selective evolutionary changes in the genetic content of closely related microorganisms.

Chemolithoautotrophic

A term used to describe organisms that use sources of chemical energy, rely on inorganic compounds (for example, H2O and H2S) for reducing power and assimilate inorganic carbon for cellular growth.

Proteorhodopsin

A photoactive, transmembrane protein that functions as a light-driven proton pump. Different forms of the protein differ in their light-absorption characteristics, which enables the absorption of light energy from different regions of the visible light spectrum. In the ocean, proteorhodopsin is found among diverse members of the Bacteria, Archaea and Eukarya.

Copiotrophic

A term used to describe an organism that is adapted to growth in habitats where nutrient concentrations are high. Such habitats are rare in the open sea but can occur at microscales, such as those in proximity to sources of organic matter (that is, living cells and detritus).

Mesopelagic

A term used to describe the vertical region of the ocean that encompasses the mid-depth (generally ∼ 200–1000 m) waters that lie between the well-lit euphotic zone and the deep bathypelagic waters. The mesopelagic waters are characterized by vanishingly low light and pronounced gradients in temperature and nutrients.

Diazotroph

A dinitrogen (N2)-fixing microorganism. The ocean contains diverse assemblages of diazotrophs, which include microscopic single-celled organisms and larger filamentous forms. These organisms rely on diverse metabolisms and are frequently found in symbiosis with other planktonic prokaryotes and eukaryotes. Diazotrophs seem to be most abundant in the upper ocean, where nutrient concentrations (specifically inorganic nitrogen) are low and sunlight, which is their primary energy source, is plentiful.

Stoichiometry

The proportions of specific nutrient elements that are found in organic compounds or dissolved in seawater. Variance in the relative proportions of these elements provides insights into specific ecological and biogeochemical processes; for example, nitrogen fixation supplies fixed cells with nitrogen but consumes phosphorus from seawater, which results in a shift in the relative proportions of these two elements in cellular material and in seawater.

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Karl, D., Church, M. Microbial oceanography and the Hawaii Ocean Time-series programme. Nat Rev Microbiol 12, 699–713 (2014). https://doi.org/10.1038/nrmicro3333

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