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  • Review Article
  • Published:

Marine microbial community dynamics and their ecological interpretation

Nature Reviews Microbiology volume 13, pages 133–146 (2015)Cite this article

Subjects

Key Points

  • The observation and analysis of marine microbial community dynamics provide insights into how microorganisms are influenced by their environment and other microorganisms.

  • The application of methods that estimate microbial populations and their dynamics over time have revealed patterns that indicate community-level resilience and, often, seasonality. This Review describes the processes that lead to the variability of ocean time series, including the factors that operate over various scales, from hours to decades, with a focus on time series of >5 years.

  • We discuss traditional and newly developed methodological and statistical techniques for analysing microbial community dynamics, including the advantages and shortcomings of each.

  • Emergent properties such as community seasonality, resilience and predictability from several studies are explored, with particular attention to their broader relevance and ecological implications. We hypothesize that what outwardly seems to be a predictable, well-regulated community is the result of numerous underlying natural ecological feedback processes among individual microorganisms, which is similar to Adam Smith's 'invisible hand' metaphor.

  • Several time series have explored pairwise ecological interactions between microorganisms that enable examination of complex ecological network associations; we discuss their possible ecological explanations and implications.

  • We define current technological developments that will help to address timeless questions of the controls and functions of marine microbial community dynamics, including the integration of top-down and bottom-up processes.

Abstract

Recent advances in studying the dynamics of marine microbial communities have shown that the composition of these communities follows predictable patterns and involves complex network interactions, which shed light on the underlying processes regulating these globally important organisms. Such 'holistic' (or organism- and system-based) studies of these communities complement popular reductionist, often culture-based, approaches for understanding organism function one gene or protein at a time. In this Review, we summarize our current understanding of marine microbial community dynamics at various scales, from hours to decades. We also explain how the data illustrate community resilience and seasonality, and reveal interactions among microorganisms.

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Figure 1: Resilience and predictability of community composition.
Figure 2: Translation of community dynamics into a microbial association network.
Figure 3: Network features change dramatically at different timescales and with the inclusion of different microorganisms.

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Acknowledgements

The authors thank present and past members of the Fuhrman Lab, especially C. Chow, and three anonymous reviewers. This work was supported by the NSF grants 1031743 and 1136818, and the Gordon and Betty Moore Foundation through Grant GBMF3779 to J.A.F.

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Authors and Affiliations

  1. Department of Biological Sciences and Wrigley Institute for Environmental Studies, University of Southern California, Los Angeles, 90089–0371, California, USA

    Jed A. Fuhrman, Jacob A. Cram & David M. Needham

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  1. Jed A. Fuhrman
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  2. Jacob A. Cram
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  3. David M. Needham
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Correspondence to Jed A. Fuhrman.

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Glossary

Phototrophic

Organisms that can transform light energy into biologically usable (chemical) forms. A photoautotroph obtains its biomass carbon from fully oxidized carbon (that is, carbon dioxide) and a photoheterotroph obtains its biomass carbon from reduced carbon (for example, organic matter).

Chemotrophic

Organisms that can obtain energy from chemical reactions. A chemoautotroph obtains its biomass carbon from carbon dioxide, and a chemoheterotroph obtains its biomass from reduced carbon.

Heterotrophic

Organisms that obtain their biomass from reduced carbon.

Microbial loop

The microbial components of the food web — such as bacteria, archaea, protists and viruses — which together process the recycling and return of dissolved organic matter back into the 'classical' food web (the food web that is more traditionally related to the transfer of particulate organic matter, including organisms).

Fronts

Boundaries in the sea between different water masses, across which environmental conditions (for example, temperature and nutrient concentrations) change abruptly, similar to weather fronts on land where there are abrupt changes in temperature and humidity.

Copiotrophic

Organisms that generally rely on relatively high concentrations of nutrients and have rapid maximum growth rates.

Grazing

In the context of plankton, grazing refers to the removal of organisms by a predatory or herbivorous organism.

Upwelling

The physical upward vertical transport of water from deeper to shallower depths (often caused by seasonal offshore winds near a coast). In the context of this Review, it refers to water and its accompanying nutrients entering the euphotic zone from below.

Allochthonous material

Material that is derived from an external source, as opposed to autochthonous material that is generated internally.

Eddies

Swirls of water motion caused by flow around objects or by instabilities inherent in the motion of density-stratified water on a rotating Earth. Ocean mesoscale eddies are typically 10–500 km in diameter.

Autoregression

Refers to the phenomenon in which samples that are collected closer to each other (in space or time) tend to be more similar to each other than those further separated.

Phytoplankton

(Also known as photosynthetic plankton). Single-cell photosynthetic organisms that form the basis of the marine food web, including cyanobacteria and many kinds of protists (such as diatoms, dinoflagellates, coccolithophores and others).

Allelopathic

An organism is termed allelopathic if it produces biochemicals that influence the growth, behaviour and reproduction of other organisms, with negative allelopathy adversely affecting the target organisms. The chemicals are generally not required for metabolism and include compounds such as antibiotics or repellants.

Stratification

The layering of water by density, which is caused by variations in temperature and salinity. As vertical mixing eliminates stratification, the existence of stratified water indicates that there is no significant vertical mixing over the stratified depth range.

El Niño Southern Oscillation

(ENSO). The effect of long-term variations in sea surface temperatures, primarily in the eastern Pacific Ocean, with anomalies lasting several months. Although the underlying causes are not fully known, it is correlated with pressure variations along the entire Pacific Basin and it affects upwelling, productivity and global weather patterns.

Pacific Decadal Oscillation

A long-term (20–30-year) oscillation of temperatures in the Pacific Ocean north of 20 degrees.

Euphotic zone

The upper layer of an aquatic water column that has sufficient light to support net photosynthesis.

Anticyclonic

A type of motion. In oceanography, it refers to the circulation of water around a region of high pressure. In the Northern Hemisphere, water rotates clockwise when viewed from above.

Mesopelagic

The middle of the ocean water column, below the euphotic zone and above the sea floor and the 'abyssal zone', which is usually defined as the water below average depth of the world ocean (approximately 4,000 m).

Estuarine outflow

Water passing from a river (low salinity) to the sea (normal ocean salinity).

Ephemeral niches

Sites at which specific environmental conditions exist for only a relatively short period of time.

Ecological niches

(Here we use the version of the concept popularized by G. E. Hutchinson). The multidimensional properties of the lifestyle of an organism or population, including the resources it uses, preferred temperatures, pressures, light levels and spectra, salinities, pH, redox state; its competitors, predators, prey, parasites, pathogens, symbionts; its alteration of its own habitat, and any other environmental factors that influence its growth and survival. The concept of an ecological species refers to a species that occupies a particular multidimensional niche that is distinct from others.

Bray–Curtis similarity

A pairwise comparison of two communities, whereby each community composition has been described by the proportions of comprising taxa, and the similarity is calculated as the total of all the shared proportions of all the taxa in both communities. It ranges from 0, when no taxa are shared, to 1, when all taxa are present in the same proportions in both communities.

Automated ribosomal intergenic spacer analysis

(ARISA). A microbial community fingerprinting approach, in which the highly variable intergenic spacer between the 16S and 18S rRNA is amplified by PCR, and the products, which vary from taxon to taxon, are separated and sized by a genetic fragment analyser.

Fingerprinting

A range of molecular genetic approaches that quickly profile the diversity of microbial communities in a sample. Instead of directly identifying individuals by their actual gene sequences, fingerprinting is based on the length of genes or sequence properties (such as the location of a restriction site), and it shows how many variants of a gene are present and in what proportions.

Tag sequencing

A high-throughput method for determining the microbial community composition in a sample via PCR and sequencing of a portion of the rRNA genes (sometimes other genes).

Lotka–Volterra

The most well-known mathematical model of predator–prey interactions, in which predator and prey usually oscillate with a time offset between them.

Ecotypes

Genetically distinct organisms that are adapted to specific environmental conditions. The term is often used in microbiology to avoid the difficulties of formally defining species.

Reverse ecology population genomics

An approach that uses genomic information from metagenomes or isolates to assess gene flow and the nature of populations and ecological units (for example, 'species').

Ecogenomic sensors

Devices that are typically used by autonomous in situ sampling systems to detect genome characteristics to facilitate the identification of organisms or other factors (such as nutrients, temperature and others).

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Fuhrman, J., Cram, J. & Needham, D. Marine microbial community dynamics and their ecological interpretation. Nat Rev Microbiol 13, 133–146 (2015). https://doi.org/10.1038/nrmicro3417

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