A novel algicidal bacterium against marine diatoms has implications for carbon and nitrogen system resource economy

Background/Question/Methods

Photosynthetic algae, including phytoplankton, are globally significant CO2 sinks and have high biotechnological potential. Their growth and efficiency are largely shaped by the microbial communities that dwell on and around them, for example heterotrophic bacteria that assimilate and remineralize algal-derived carbon and nitrogen. Our previous work has shown that bacteria influence algal productivity, either positively via mutualism or negatively via antagonism, through complex interactions including exchanges of secondary metabolites. Here, we document a novel algicidal bacterium that lyses the biofuel-relevant marine diatom Phaeodactylum tricornutum, crashing laboratory cultures in days. The algicidal bacterium was sourced from an estuarine water sample containing a whole bacterial community and maintained in a laboratory enrichment. This novel bacterium cannot be isolated using traditional microbiological laboratory techniques, thus we used molecular approaches (16S rRNA sequencing, FISH, metagenomics, metatranscriptomics) and unique resources (confocal microscopy, NanoSIMS isotope tracing) with the objective of characterizing its identity, strategy, and mechanism of parasitism. We hypothesized that the bacterium is dependent on the diatom host and can incorporate host-derived organic carbon and nitrogen. In the process of lysing cells, we hypothesized that the bacterium would affect microalgal carbon fixation and stimulate changes in the system resource economy and surrounding microbial community activity.

Results/Conclusions

The algicidal bacterium resides within a community enrichment of 55 bacterial taxa and increases in relative abundance in conjunction with diatom P. tricornutum decline. Based on phylogeny of a 16S gene recovered from rRNA sequencing and metagenome-assembled-genomes (MAGs), we identified this bacterium as a previously uncharacterized Rickettsiales and the first known algicidal bacterium of this taxonomic group. Through super-resolution confocal microscopy and fluorescence in situ hybridizations (FISH), we show that this Rickettsiales attaches in high density to host diatom cells just prior to the population crash. Interestingly, unlike other Rickettsiales that are obligate intracellular organisms, this bacterium is an extracellular parasite of microalgae that can survive free-living. Metabolic predictions from the MAG confirmed genomic capacity for aggregation and attachment to host cells using pili along with a full type IV secretion system. Our stable isotope tracing experiments with 13C and 15N show that during attachment and lysis of host cells, the bacterium can incorporate algal-derived carbon and nitrogen. Future work will validate genome and metabolic model predictions using metatranscriptomes of both the bacterial community and algal host P. tricornutum. These data contribute to our understanding of poorly characterized algicidal bacteria in the environment and more broad understanding of algal-bacterial interactions.