Mutation, Mutation, Mutation: Roseobacter needed a lifestyle change

Rapid adaptation of organisms in stressful environments is vital for survival, especially with today’s warming climate. Marine bacteria have shown that they can quickly adapt to such adverse conditions; given their intrinsic function in global biogeochemical cycling, it is important to understand any ramifications of such adaptations on the physiology and lifestyle of these organisms. 

Kent et al. (2018) used experimental evolution to assess the rapid adaptation in physiology and lifestyle of a member of the abundant marine bacterial clade Roseobacter, under chronic high temperature conditions (33˚C). Roseovarius sp. TM1035 were isolated from a Chesapeake Bay dinoflagellate culture and propagated for 500 generations under optimal (25˚C) and high (33˚C) temperature regimes.

Through genomic and physiological assessment, they found that High Temperature-adapted Lines (HTLs) of Roseobacter had a higher number of gene mutations. A restriction enzyme assay was used to quantify these changes in sequence and allele frequency in the final colonies, compared to the initial ancestor isolated, and calculate the selection rate constant. Mutations found included alterations in genes controlling gas transfer, growth rate, exopolysaccharide secretion and quorum sensing. 

These mutations corresponded to the increased production of biofilm at high temperatures at the water’s surface. This was quantified between experimental lines, with the aid of a crystal violet stain and a spectrophotometer. These results are particularly interesting as an increase in biofilm formation could alter the community structure and composition of the sea-surface microlayer: a vital component particularly of the open ocean ecosystem. It is intrinsic in governing gas exchange, aerosolization and production of Cloud-condensation nuclei, affecting many important ocean processes. If the results of this paper are applicable to a real-world scenario of ocean warming, the precise nature of the sea-surface microlayer may be destabilised. However, some may argue that high temperature events in the ocean are likely to be short term; temperature would fluctuate over 500 generations in a more natural system, potentially yielding different results than seen in this highly controlled experiment.

In addition to increased biofilm formation, some colonies also displayed wrinkly morphotypes, and both these observations were almost entirely confined to the HTLs. Furthermore, the HTL wrinkly morphotypes were experimentally competed against the ancestor and Low Temperature-adapted Lines (LTL) and this was used to independently calculate the selection rate constant. The results yielded from this were consistent to those from the restriction enzyme assay.

The changes in physiology and lifestyle were linked to the thermally-driven decline in oxygen tension. This was assessed in a secondary investigation, in which the HTLs grew relatively better under conditions of low gas transfer compared to the LTLs and ancestor lines. Increased biofilm production may facilitate access to oxygen, sequestering it into a relatively stable matrix, therefore allowing the Roseobacter to grow more efficiently in the thermally-limited low oxygen conditions. HTLs were also shown to have an increased selection rate constant under low oxygen tension, suggesting that this stress induced directional selection: a means for quick adaptation. Kent et al. highlight that the warming climate presents multi-faceted challenges, and indirect effects of adaptation may initiate significant modification to lifestyle and ecosystem function of ubiquitous and crucial marine microorganisms; understanding this is the key to more accurately predicting the effect of warming on our microbial seas. The rapid nature of the adaptations observed here are simultaneously comforting and alarming. While it seems that the survival of a major biogeochemical powerhouse is not at risk, the significant modification of its lifestyle could have severe implications for the delicately balanced sea-surface micro layer: yet another facet of ocean warming to be considered.

Definitions:

Quorum sensing: The ability of organisms to sense and respond to nearby cell density; this can include the alteration of phenotype expression according to the density of the local population. In turn it can inform biofilm formation along with virulence factor expression, motility and many more processes.

Reference:

Kent, A. G., Garcia, C. A., & Martiny, A. C. (2018). Increased biofilm formation due to high-temperature adaptation in marine Roseobacter. Nature microbiology, 3(9), 989.