The identification of an exchange of nutrients and signalling molecules between a planktonic alga and a bacterium demonstrates that targeted mutualistic interactions occur across domains of life in the oceans. See Letter p.98
The sunlit surface waters of the ocean are inhabited by unicellular algae that perform approximately half of our planet's photosynthesis1 and are crucial for sustaining Earth's atmosphere. These phytoplankton live in a complex milieu with other microorganisms, many of which rely on the products of algal photosynthesis for growth2. Although chemical cross-talk between the microorganisms that inhabit the human body or the root zone of plants is well established3,4,5, it is difficult to imagine similarly intimate interactions in dilute ocean environments. Indeed, an enduring mystery of marine ecology and carbon-cycle science is whether there are specific mutualistic relationships between ocean microbes or whether exchanges are largely the result of random encounters between released compounds and free-living cells. On page 98 of this issue, Amin et al.6 describe how a widespread free-living alga and a bacterium engage in a targeted exchange of nutrients and metabolites. This includes transfer of a hormone found in land plants, although neither organism is evolutionarily related to plants.
The diatoms are a group of eukaryotic algae that have important roles in primary production (the generation of organic carbon from carbon dioxide) and in marine food chains7. Amin et al. studied the diatom Pseudo-nitzschia multiseries, which has a complicated ecological role because, as well as being a primary producer, it can produce the neurotoxin domoic acid, which causes amnesic shellfish poisoning in humans and other consumers as its concentration is increased up the food chain. In the current report, the authors focus on how P. multiseries growth is affected by the activities of bacteria, the identities of bacteria that augment its growth, and how the alga or bacterium may manipulate the other to its own benefit.
To illuminate these interactions, Amin et al. used an impressive array of co-culturing experiments, genome sequencing, RNA-transcript analyses and metabolite profiling in studies extending from the laboratory into the wild. In characterizing algae–bacteria relationships, the researchers found that, among 49 bacterial strains isolated from P. multiseries cultures, members of the genus Sulfitobacter had the largest positive effect on the alga's growth. Further testing using Sulfitobacter strain SA11 showed algal growth enhancement occurred for just two of four P. multiseries strains examined, and there was no observable effect for another diatom genus. Perhaps more surprisingly, enhancement of bacterial growth was also highly specific, with only some strains of P. multiseries increasing the Sulfitobacter's growth. Phytoplankton exude organic carbon molecules that are assimilated by bacteria, and themselves use nutrients remineralized by bacteria2, but there is little evidence that greater specificity defines these exchanges. The findings presented unambiguously show that more nuanced interactions occur.
The authors characterized the mutualistic relationship between P. multiseries strain PC9 and Sulfitobacter strain SA11 in further detail (Fig. 1). Gene-expression analysis indicated that SA11 uses taurine, an organic compound excreted by the diatom, as a carbon source. The breakdown of taurine yields sulfite, which is notable because several Sulfitobacter strains oxidize sulfites as an energy source8. SA11 also responded to another diatom-derived organosulfur compound, dimethylsulfoniopropionate (DMSP), by upregulating a gene that degrades it. By this mechanism, SA11 presumably gains another carbon source, acrylate, while releasing the volatile gas dimethylsulfide (DMS). DMS is considered a climate-active gas because it is oxidized to sulfate particles around which water vapour can condense9, although its contribution to cloud formation is minor in the upper atmosphere where the largest cloud-related influences on climate occur10. Collectively, the study results suggest that compound exchanges and signalling such as those observed in this diatom–bacteria network represent an important link in global cycling of both carbon and sulfur.
Concurrent with its assimilation of diatom-derived organic carbon, SA11 secretes ammonium — a heavily scavenged commodity in low-nutrient marine settings because it is the most reduced form of nitrogen available. By outsourcing nitrate reduction to the bacterium and aquiring other molecules from it, the diatom can divert cellular resources towards other processes, such as growth. Indeed, the authors' transcriptome analyses indicate that, in the presence of SA11, P. multiseries increases expression of genes associated with photosynthesis and carbon fixation, presumably to support the higher growth rates observed, as well as to provide organic carbon exudates for the bacterial partner.
But the emerging picture of a diatom–bacterium partnership is more complex than this simple resource swap. Amin et al. postulate that the exchanges between these free-living microbes are coordinated through cycling of the hormone indole-3-acetic acid (IAA) and the amino acid tryptophan. Best known for its use by terrestrial plants to direct developmental processes such as the growth of new shoots, IAA also has a role in signalling between soil bacteria and plants4. The researchers demonstrate that P. multiseries and Sulfitobacter SA11 secrete tryptophan and IAA, respectively. Moreover, they show that addition of synthetic IAA to cultures of P. multiseries stimulates the diatom's growth, but that the effect is significantly greater when the IAA-producing bacterium itself is present. This indicates that, although IAA promotes diatom cell division, additional unidentified factors are involved in the positive feedback loop that results in major diatom growth enhancement. The authors also detected IAA in water samples from five North Pacific sites and present transcriptomic evidence from field samples for multiple IAA biosynthesis pathways, each incorporating different precursor molecules. Thus, it seems that IAA signalling occurs across domains of life in both the terrestrial and marine biospheres and is probably an ancient mechanism of organismal communication.
Amin and colleagues' study represents a substantial step forward for understanding the complex network of interactions between phytoplankton and bacteria and provides a springboard for development of hypotheses on cross-talk between marine microbes. For example, the extreme interaction specificity observed suggests that the consortium of bacteria residing in a particular habitat may be a major force in structuring the local phytoplankton community, or vice versa. Moreover, it seems reasonable to speculate that, in addition to IAA and tryptophan, other signalling molecules participate in inter- or intradomain communication among marine microbes.
Perhaps the most pressing question we are left with is when and where such interactions occur. Symbioses between diatoms and nitrogen-gas-fixing cyanobacteria are known11, and bacterial attachment to diatoms is often reported during algal blooms and in the bloom senescence phase12,13. For decades, scientists have also speculated on the potential influence of microscale variability of resources in marine environments14 and on the significance of the phycosphere15 — a zone around algal cells considered analogous to the root zone of plants. Concentrations of algal secreted compounds are much higher in the phycosphere than in nearby sea water, owing to the basic physics of the diffusive boundary layer surrounding the cell, thus promoting growth of bacteria in this layer13,15.
Amin and colleagues' results suggest that the specific growth-enhancing interactions observed occur in the phycosphere, but the sampling methods and quantitation techniques needed to directly assess the physical nature of these associations are still lacking. Exciting times are ahead as scientists develop techniques to examine the physical intricacies of these mutualistic relationships, their prevalence and structuring roles in marine microbial communities, and how they might shift under environmental change.Footnote 1
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