Heterotroph Interactions Alter Prochlorococcus Transcriptome Dynamics during Extended Periods of Darkness

Abstract

Prochlorococcus is the most abundant photosynthetic organism on the planet. These cells play a central role in the physiology of surrounding heterotrophs by supplying them with fixed organic carbon. It is becoming increasingly clear, however, that interactions with heterotrophs can affect autotrophs as well. Here we show that such interactions have a marked impact on the response of Prochlorococcus to the stress of extended periods of darkness, as reflected in transcriptional dynamics. These data suggest that diel transcriptional rhythms within Prochlorococcus, which are generally considered to be strictly under the control of light quantity, quality, and timing, can also be influenced by biotic interactions. Together, these findings provide new insights into the importance of microbial interactions on Prochlorococcus physiology and reveal conditions where heterotroph-derived compounds may support autotrophs—contrary to the canonical autotroph-to-heterotroph trophic paradigm.

Genomic, metabolic and phenotypic variability shapes ecological differentiation and intraspecies interactions of Alteromonas macleodii

“…Comparison with prior transcriptomic data 59 showed that interactions of MIT1002 with Prochlorococcus involve several unique genes (Table S4). For instance, differential regulation of unique chemotaxis-, motility-and biofilm-related genes in co-culture may strengthen physical associations 70 whereas upregulation of a phytase gene might enhance phosphorus acquisition 71 .…”

“…In addition to plasmids, ecological differentiation also relates to varying abilities for microbial interactions 57 . In this context, strains MIT1002 and EZ55 are naturally associated with Prochlorococcus cyanobacteria, to whom they establish mutualistic relationships by alleviating oxidative stress or nutrient limitation during extended periods of darkness [58][59][60][61] . Here, we demonstrate additional features that may support their co-existence.…”

“…The Alteromonas-Prochlorococcus interplay may be further strengthened by metabolic interrelations, as FT-ICR-MS revealed that MIT1002 and EZ55 secrete ecologically relevant exometabolites Table 1). Secretion of methyl-tryptophan and methyl-indolepyruvate may explain the differential regulation of tryptophan biosynthesis in Prochlorococcus when co-cultured with A. macleodii 64,65 , especially under restricted photosynthesis 59 . Secretion of asparagine and glutamine (Table 1) indicates exchange of further amino acids, coincident with upregulation of related importers in Prochlorococcus when co-cultured 64 .…”

Identification of circadian rhythms in Nannochloropsis species using bioluminescence reporter lines

“…It has been hypothesized that an hourglass oscillator that is reset every day is sufficient for these Prochlorococcus species because they originate from southern latitudes where they do not experience large changes in daylength, and their marine environment is more stable than freshwater habitats (Mullineaux and Stanewsky, 2009). A recent study shows that diel rhythms are stronger in Prochlorococcus in co-culture with a heterotrophic bacterium, suggesting that biotic interactions can help to maintain oscillations in plankton communities (Biller et al, 2018). Experiments using arrhythmic and weakly rhythmic mutants in S. elongatus indicate that lines with a damped oscillator grow better than the wild type under light/dark cycles (Woelfle et al, 2004), which suggests that a robust clock is not required for optimal growth under diel conditions.…”

Identification of circadian rhythms inNannochloropsisspecies using bioluminescence reporter lines

“…It has been hypothesized that an hour-glass oscillator that is reset every day is sufficient for these Prochlorococcus species because they originate from southern latitudes where they do not experience large changes in daylength, and their marine environment is more stable than fresh water habitats (Mullineaux and Stanewsky 2009). A recent study shows that diel rhythms are stronger in Prochlorococcus in co-culture with a heterotrophic bacterium suggesting that biotic interactions can help maintain oscillations in plankton communities (Biller et al , 2018). Experiments using arrhythmic and weakly rhythmic mutants in S. elongatus indicate that lines with a damped oscillator grow better than the wild type under light/dark cycles (Woelfle et al , 2004) which suggests that a robust clock is not required for optimal growth under diel conditions.…”