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Bacterial Blooms: The social life of cyanobacteria

  1. Conrad W Mullineaux  Is a corresponding author
  2. Annegret Wilde
  1. School of Biological and Chemical Sciences, Queen Mary University of London, United Kingdom
  2. Institute of Biology III, University of Freiburg, Germany
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Cite this article as: eLife 2021;10:e70327 doi: 10.7554/eLife.70327

Abstract

The cyanobacterium Synechocystis secretes a specific sulphated polysaccharide to form floating cell aggregates.

Main text

Cyanobacteria are ancient and extremely versatile organisms that can be found in nearly every ecosystem on Earth, in particular lakes, rivers and oceans. Like plants and algae, they produce oxygen and use sunlight as an energy source.

Some cyanobacteria – even single-celled ones – show striking collective behaviours and form colonies (or ‘blooms’) that can float on water and have important ecological roles. For instance, billions of years ago, communities of marine Paleoproterozoic cyanobacteria could have helped create the biosphere as we know it by burying carbon compounds and allowing the initial build-up of oxygen in the atmosphere (Kamennaya et al., 2018). On the other hand, toxic cyanobacterial blooms are an increasingly issue for society, as their toxins can be harmful to animals (Huisman et al., 2018). Extreme blooms can also deplete water of oxygen and reduce sunlight and visibility, thereby compromising the feeding and mating behavior of light-reliant species.

It has been unclear why and how cyanobacteria form communities. Aggregation must divert resources away from the core business of making more cyanobacteria, as it generally involves the production of copious quantities of extracellular material. In addition, cells in the centre of dense aggregates can also suffer from both shading and shortage of nutrients (Conradi et al., 2019; Enomoto and Ikeuchi, 2020). So, what advantage does this communal life bring for cyanobacteria?

Now, in eLife, Masahiko Ikeuchi of the University of Tokyo and colleagues – including Kaisei Maeda as first author – report new insights into how cyanobacteria form blooms (Maeda et al., 2021). Using the widely studied cyanobacterium Synechocystis, they identified a set of genes that regulate the production and export of sulphated polysaccharides, chains of sugar molecules modified with sulphate groups that can often be found in marine algae and animal tissue. Many bacteria generate extracellular polysaccharides, but sulphated ones have only been seen in cyanobacteria.

Maeda et al. showed that the sulphated polysaccharide in Synechocystis, which they named Synechan, helps the cyanobacterium to form buoyant aggregates by trapping oxygen bubbles in the slimy web of cells and polysaccharides. This suggests that a major purpose for the production of Synechan is buoyancy.

Previous studies on Synechocystis have shown that type IV pili, which decorate the surface of cyanobacteria, also play a role in forming blooms (Allen et al., 2019; Conradi et al., 2019). These retractable and adhesive protein fibres are important for motility, adhesion to substrates and DNA uptake (Schuergers and Wilde, 2015). The formation of blooms may require both type IV pili and Synechan – for example, the pili may help to export the polysaccharide outside the cell. Indeed, the activity of these protein fibres may be connected to the production of extracellular polysaccharides in filamentous cyanobacteria (Khayatan et al., 2015). A more obvious answer would be that pili help to build the aggregates by binding the cells with each other or with the extracellular polysaccharide. As with other kinds of bacteria (Adams et al., 2019), certain components of the pili may allow cyanobacteria from the same species to recognise each other and make initial contacts, which are then stabilised by building a mass of extracellular polysaccharide.

The ‘bubble flotation’ mechanism identified by Maeda et al. joins a range of known strategies that enable cyanobacteria to control their buoyancy, such as using gas vesicles or accumulating carbohydrate ballasts (Figure 1; Kromkamp and Walsby, 1990). Type IV pili on their own could also control the position of marine cyanobacteria in the water column by regulating viscous drag (Aguilo-Ferretjans et al., 2021). Extracellular polysaccharide appears to be a multipurpose asset for cyanobacteria, from floatation device to food storage, defence mechanism and mobility aid (Khayatan et al., 2015). Cyanobacteria can make surprisingly complex and diverse lifestyle choices, and the role of slime in their social life calls for further exploration.

Collective behaviour and lifestyle choices in single-celled cyanobacteria.

Bacteria can stay in suspension as individual cells, adhere collectively to surfaces to form biofilms, passively sediment, or flocculate to form suspended aggregates. Cyanobacteria are able to produce sulphated polysaccharides (yellow haze surrounding clumps of cells) that enable them to form floating aggregates. Maeda et al. discovered that the oxygen produced by the cyanobacteria becomes trapped in the network of polysaccharides and cells, enabling the microorganisms to form buoyant blooms. It is thought that specific protein fibres known as pili (represented as lines radiating from the cells) may act as an additional way to link cells to each other or onto surfaces. Some cyanobacteria also use sophisticated intracellular gas vesicles as floating aids.

It remains to be seen if Synechan production in nature would serve to segregate cyanobacteria away from other species, including dangerous predators; or whether it may help to build a floating microbial community where multiple, metabolically diverse species can cooperate. We know so little about the real life of Synechocystis outside the laboratory that both ideas are equally possible.

References

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Author details

  1. Conrad W Mullineaux

    Conrad W Mullineaux is in the School of Biological and Chemical Sciences, Queen Mary University of London, London, United Kingdom

    For correspondence
    c.mullineaux@qmul.ac.uk
    Competing interests
    No competing interests declared
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7194-9916
  2. Annegret Wilde

    Annegret Wilde is in the Institute of Biology III, University of Freiburg, Freiburg, Germany

    Competing interests
    No competing interests declared
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0935-8415

Publication history

  1. Version of Record published: June 16, 2021 (version 1)

Copyright

© 2021, Mullineaux and Wilde

This article is distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use and redistribution provided that the original author and source are credited.

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Further reading

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    Sofiene Seef et al.
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    Myxococcus xanthus, a soil bacterium, predates collectively using motility to invade prey colonies. Prey lysis is mostly thought to rely on secreted factors, cocktails of antibiotics and enzymes, and direct contact with Myxococcus cells. In this study, we show that on surfaces the coupling of A-motility and contact-dependent killing is the central predatory mechanism driving effective prey colony invasion and consumption. At the molecular level, contact-dependent killing involves a newly discovered type IV filament-like machinery (Kil) that both promotes motility arrest and prey cell plasmolysis. In this process, Kil proteins assemble at the predator-prey contact site, suggesting that they allow tight contact with prey cells for their intoxication. Kil-like systems form a new class of Tad-like machineries in predatory bacteria, suggesting a conserved function in predator-prey interactions. This study further reveals a novel cell-cell interaction function for bacterial pili-like assemblages.

    1. Medicine
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    Alexander O Pasternak et al.
    Research Article Updated

    Background:

    It remains unclear whether combination antiretroviral therapy (ART) regimens differ in their ability to fully suppress human immunodeficiency virus (HIV) replication. Here, we report the results of two cross-sectional studies that compared levels of cell-associated (CA) HIV markers between individuals receiving suppressive ART containing either a non-nucleoside reverse transcriptase inhibitor (NNRTI) or a protease inhibitor (PI).

    Methods:

    CA HIV unspliced RNA and total HIV DNA were quantified in two cohorts (n = 100, n = 124) of individuals treated with triple ART regimens consisting of two nucleoside reverse transcriptase inhibitors (NRTIs) plus either an NNRTI or a PI. To compare CA HIV RNA and DNA levels between the regimens, we built multivariable models adjusting for age, gender, current and nadir CD4+ count, plasma viral load zenith, duration of virological suppression, NRTI backbone composition, low-level plasma HIV RNA detectability, and electronically measured adherence to ART.

    Results:

    In both cohorts, levels of CA HIV RNA and DNA strongly correlated (rho = 0.70 and rho = 0.54) and both markers were lower in NNRTI-treated than in PI-treated individuals. In the multivariable analysis, CA RNA in both cohorts remained significantly reduced in NNRTI-treated individuals (padj = 0.02 in both cohorts), with a similar but weaker association between the ART regimen and total HIV DNA (padj = 0.048 and padj = 0.10). No differences in CA HIV RNA or DNA levels were observed between individual NNRTIs or individual PIs, but CA HIV RNA was lower in individuals treated with either nevirapine or efavirenz, compared to PI-treated individuals.

    Conclusions:

    All current classes of antiretroviral drugs only prevent infection of new cells but do not inhibit HIV RNA transcription in long-lived reservoir cells. Therefore, these differences in CA HIV RNA and DNA levels by treatment regimen suggest that NNRTIs are more potent in suppressing HIV residual replication than PIs, which may result in a smaller viral reservoir size.

    Funding:

    This work was supported by ZonMw (09120011910035) and FP7 Health (305522).