How mutualisms arise in phytoplankton communities: building eco-evolutionary principles for aquatic microbes

Abstract

Extensive sampling and metagenomics analyses of plankton communities across all aquatic environments are beginning to provide insights into the ecology of microbial communities. In particular, the importance of metabolic exchanges that provide a foundation for ecological interactions between microorganisms has emerged as a key factor in forging such communities. Here we show how both studies of environmental samples and physiological experimentation in the laboratory with defined microbial co-cultures are being used to decipher the metabolic and molecular underpinnings of such exchanges. In addition, we explain how metabolic modelling may be used to conduct investigations in reverse, deducing novel molecular exchanges from analysis of large-scale data sets, which can identify persistently co-occurring species. Finally, we consider how knowledge of microbial community ecology can be built into evolutionary theories tailored to these species' unique lifestyles. We propose a novel model for the evolution of metabolic auxotrophy in microorganisms that arises as a result of symbiosis, termed the Foraging-to-Farming hypothesis. The model has testable predictions, fits several known examples of mutualism in the aquatic world, and sheds light on how interactions, which cement dependencies within communities of microorganisms, might be initiated.

Keywords: Eco-evolutionary dynamics; Foraging-to-Farming hypothesis; metabolite exchange; metagenomics; microbial communities; mutualism; phytoplankton; vitamins.

Figure 1

Unicellular organisms dominate the eukaryotic lineages. A schematic diagram of the eukaryotic tree of life showing the major groups (Dorrell & Smith (2011); Burki 2014). At present the positions of the Haptophytes, Telonemids, Cryptomonads and Centrohelids remain uncertain (Incertae sedis). Multicellularity has evolved only seven times (highlighted with filled circles); all other lineages are essentially microbial.

Figure 2

Schematic of phytoplankton lifestyles. Ecologically significant groups, including diatoms, bloom and are subject to viral lysis and grazing by heterotrophic zooplankton. This releases organic nutrients into solution, which both cyanobacteria and algae can utilise via mixotrophy. Moreover, many algae such as dinoflagellates consume bacterial prey via phagotrophy, resulting in net CO₂ release and O₂ consumption. In addition to these trophic processes is a complex series of interactions, or symbioses, which have shaped the ecology and evolution of microbes in aquatic communities. Many examples of mutualism are known, where algae supply fixed carbon (photosynthate) in exchange for specific nutrients such as vitamins. Parasitism can also arise, as in the case of senescing haptophytes, where bacterial partners that were initially mutualistic produce algaecides to accelerate the process, indicating that interactions can be dynamic. Intimate physical associations, in the form of endosymbiosis, such as between the amoeboid protistan radiolarians and haptophytes, are also frequent.

Figure 3

Microbial systems with well‐characterised metabolic exchanges. These have been used to validate the SMETANA algorithm devised by Zelezniak et al. (2015). In each case solid arrows represent known exchanges tested in physiological studies and dotted arrows mark potential novel interactions predicted by SMETANA. (a) A three‐species community based on cellobiose degradation (Miller et al. 2010). SMETANA predicts that pyruvate and hydrogen may also be delivered to G. sulfurreducens by C. cellulolyticum. (b) An algal‐fungal mutualism between C. reinhardtii and Saccharomyces cerevisiae (Hom & Murray 2014). As well as refining the likely forms of N and S that are exchanged, SMETANA predicted that during co‐culture growth aspartate, glutamine and serine could also be delivered from the yeast to the alga.

Figure 4

Black Queen Hypothesis (BQH). The Black Queen refers to the Queen of Spades in the card game Hearts, where players try to avoid ending up with this card, since it carries the greatest number of negative points. In the microbial community illustrated, the ability to detoxify H₂O₂ is analogous to the Queen of Spades, because it requires katG, an enzyme with a high Fe cost. Helper bacteria, such as Alteromonas sp. act as a sink for H₂O₂ and keep concentrations low enough for Prochlorococcus and other members of the aquatic community, including the numerically dominant heterotrophic Candidatus Pelagibacter ubique, to survive. Prochlorococcus is the photosynthetic producer in the system, fixing carbon that is made available to the other species in the community.

Figure 5

Evolution of B12 auxotrophy in algae, an example of the Foraging‐to‐Farming hypothesis. Algae with both isoforms of methionine synthase (METE and METH) are unhindered in the absence of B12 (Helliwell et al. 2011), but remain facultative users of the vitamin if available, much like foragers that take advantage of sporadic resources in their environment. If a persistent supply of the vitamin is available for sufficient time, for example from surrounding loosely associated bacteria, the METE gene will be repressed and may be lost, so that the alga is now completely dependent on bacteria for survival. However, fluctuating environmental conditions may mean that vitamin B12 becomes scarce. In such circumstances algae that release a carbon source will actively maintain a viable population of bacteria, and will consequently have a selective advantage over those that do not. Here, ‘farming’ the bacteria for the resource becomes an evolutionarily stable strategy, turning a previously loose interaction into an obligate one.