Enhanced biofilm formation aids adaptation to extreme warming and environmental instability in the diatom Thalassiosira pseudonana and its associated bacteria

Abstract

Recent studies have highlighted the capacity of marine diatoms at the foundation of ocean food webs and biogeochemical cycles to respond to environmental change. These responses are a combination of physiological acclimation and evolutionary responses. The latter occur rapidly within a few hundred generations (translating to a scale of months to years), due to the large standing genetic variation and short generation times of diatom populations. Studies are usually carried out on diatom species in their planktonic state, but this may constitute a stark oversimplification: diatoms readily form biofilms in the water column of shallow coastal areas, where biofilm formation affects carbon export, and in the benthos, where biofilms contribute significantly to sediment stability. Here, I have carried out a 400‐generation selection experiment, where I evolved the diatom Thalassiosira pseudonana and its associated bacteria. Bacteria and diatom were cultured in their planktonic form, and under strong selection for rapid biofilm formation in temperature and nutrient regimes differing in their severity and stability. I find that biofilm formation is enhanced under mild warming and rapid thermal fluctuations but not under extreme warming regardless of nutrient availability. Evolutionary responses are slower in biofilms under benign conditions but speed up under extreme and fluctuating conditions. Taxonomic composition of the associated bacteria is driven by the temperature selection regime in biofilms but not in planktonic samples. I also show that T. pseudonana, when selected for biofilm formation, presents predictable and sequential morphologies that are not usually observed in planktonic T. pseudonana.

Temperature fluctuations in a warmer environment: impacts on microbial plankton

“…The studies performed have considered either short-term scales (i.e. days), which represent acute/stress responses to the environmental drivers assayed 42 , 44 , or mid-term scales, that is, those that allow organisms’ acclimation 43 , 45 , 46 ( Table 1 ). Evolutionary responses over longer time scales to the interacting effect of warming and fluctuating temperature are still underrepresented 47 ; however, it is known that thermal adaptation mediated by trait selection during evolutionary change can reverse short- and mid-term effects of constant warming on metabolic rates 48 .…”

“…Superscript numbers in response variables represent studies where interactive effects of temperature fluctuations and warming were tested. Sources are 1 Urrutia-Cordero et al 50 , 2 Rasconi et al 45 , 3 Kling et al 44 , 4 Schaum et al 43 , 5 Schaum et al 46 and 6 Wang et al 42 . Bsi represents biogenic silica, a proxy for diatom-specific rates, and PIC and POC are particulate inorganic and organic carbon, respectively.…”

“…Temperature fluctuations have been shown to accentuate, attenuate, and even reverse the effect of warming on different properties and processes at the population and community level ( Table 1 ). For instance, researchers have found a negative synergistic effect of the warming × fluctuating temperature interaction on gross photosynthesis 43 and phytoplankton evenness 45 but also a positive synergistic effect on microbial biofilm formation and phytoplankton growth 46 . Other reports indicate that temperature fluctuations can attenuate the positive effect of warming on cyanobacterial biomass production and recruitment 50 or reverse the warming effect on carbon and nitrogen quotas 43 .…”

GPCR Genes as Activators of Surface Colonization Pathways in a Model Marine Diatom

“…Particularly, biofouling on ships increases fuel and maintenance costs significantly ( Salta et al., 2013 ). Conversely, surface colonization and biofilm formation have substantial physiological advantages for microalgae in response to stress conditions and also play important roles in microbial adaptation to fluctuations in marine environments ( Dang and Lovell, 2016 ; Schaum, 2019 ).…”

Presence of a resident species aids invader evolution

“…See e.g. [38] To assess whether invaders evolved in co-culture had adapted to the novel salinity, the 460 presence of the resident species, or both, we passed all co-cultured samples through a 5µm 461 nitrocellulose filter, allowing Ostreococcus cells to pass, while Chlamydomonas cells 462 remained on the filter, from which they could be rinsed off. Samples were then inspected 463 under the microscope and flow cytometric data was again used as above to ensure a good 464 separation of the two species.…”