Happily never after: the relationship between the marine microalgae Emiliania huxleyi and the roseobacter Phaeobacter gallaeciensis

Misfortune tests the sincerity of friends – or so thought the Greek fabulist Aesop two millennia ago. The notion of this notorious human trait has grown immense popularity and has been adopted in numerous storylines. This time, however, we’ll take a slightly different approach to it.

The main protagonists in this narrative are the marine microalgae Emiliania huxleyi and the roseobacter Phaeobacter gallaeciensis. E.huxleyi is a ubiquitous coccolithophore, which plays an important role in global carbon cycling by removing CO₂ from the ocean and sequestering it as CaCO₃. It forms massive blooms during which its population expands in great densities over vast areas of the upper ocean (Holligan et al. 1993). The discovered correlation between the microalgal blooms and the roseobacter predominance has prompted Seyedsayamdost et al. (2011) to research deeper into their relationship.

In the first, mutualistic, phase of the interaction P.gallaeciensis synthesizes phenylacetic acid, an auxin which promotes algal growth. It also produces the antibiotic tropodithietic acid (TDA) and thiotropocin which protect the algal host from bacterial pathogens. E.huxleyi, on the other hand, provides the roseobacter with nutrients and an ideal surface for colonization. However, this happy relationship is not meant to last, and the honeymoon phase comes to an end as P.gallaeciensis transforms into a pathogen and kills E.huxleyi. P-coumaric acid (pCA), a lignin breakdown product generated by E.huxleyi, causes P.gallaeciensis to start producing toxins- algaecides, called roseobacticides. As pCA could be interpreted either as algal senescence or as increased algal population density, this rapid shift may occur to give the bacteria access to the food source provided by the aging algae cells, and to give it a chance to find a new healthy host. Seyedsayamdost et al. (2011) also suggests that the duplicitous lifestyle of P.gallaeciensis may be caused by the compliance of phenylalanine. Both tropone and phenylacetic acid are synthesized from phenylalanine, as is pCA, the induction signal and virtually all the components of cell wall lignin.

Beyersmann et al. (2017), on the other hand, considers TDA to be the key component to induce the switch from mutualism to pathogenesis, because of its dual function as an antibiotic and a quorum sensing (QS) mediator in the bacterium Phaeobacter inhibens. Quorum sensing is a type of cell-to-cell communication mediated by signaling molecules and used to coordinate gene expression according to the density of the local population (Marx 2014). The study proposes that the attachment of P.inhibens on its host is reduced by the activation of QS, after which biofilm-associated genes are down-regulated, which results in dispersion of the roseobacter. In a more recent approach to the topic Bramucci et al. (2018) discovered there is a dependence of the algaecidal activity of P.inhibens on the algal cell type of the host. They found that P.inhibens selectively kills two from the three examined host cell types. These cell types, however, differ from the ones targeted by algaecidal viruses. The study also claims that P.inhibens doesn’t use a roseobacticide-dependent mechanism (as described in Seyedsayamdost et al. (2011)) and must be therefore producing additional algaecidal compounds or virulence factors to kill E.huxleyi.

Now the pure moral of this story is that abandoning your friends, because they are old or sick, is indeed spineless. Yet scientifically speaking there are two key points in this review to take home: algae-bacteria interactions play an essential role in shaping species composition in pelagic environments and they are largely unexplored. As we can see bacteria have the ability to influence the microalgal cell-type composition by selective pathogenesis, thereby altering its populations and its bloom-bust lifestyle. These novel findings have a great potential in aiding us tackle microalgae-induced issues, such as harmful algal blooms (HABs). However, we still have a long way to go, until we can fully grasp the processes driven in and from bacteria in their interactions with algae.

Reviewed paper:

Seyedsayamdost, M. R., Case, R. J., Kolter, R., and Clardy, J. (2011). The Jekyll-and-Hyde chemistry of Phaeobacter gallaeciensis. Nat. Chem. 3, 331–335. doi: 10.1038/nchem.1002

References:

Beyersmann, P. G., Tomasch, J., Son, K., Stocker, R., Göker, M., Wagner-Döbler, I., et al. (2017). Dual function of tropodithietic acid as antibiotic and signaling molecule in global gene regulation of the probiotic bacterium Phaeobacter inhibens. Sci. Rep. 7, 1–9. doi: 10.1038/s41598-017-00784-7

Bramucci, A., Labeeuw, L., Orata, F. D., Ryan, E. M., Malmstom, R. R., Case, R. J. (2018). The bacterial symbiont Phaeobacter inhibens shapes the life history of its algal host Emiliania huxleyi. Front. Mar. Sci., 29 May 2018. doi: 10.3389/fmars.2018.00188

Holligan, P.M., Groom, S.B., Harbour, D.S., 1993. What controls the distribution of the coccolithophorid Emiliania huxleyi in the North Sea? Fish. Oceanogr. 2, 175-183.

Marx, V., 2014. Stop the microbial chatter. Nature 511, 493–497