Exploring the Phaeosphere: characterizing the microbiomes of Phaeocystis antarctica colonies from the coastal Southern Ocean and laboratory culture

Abstract

Interactions between phytoplankton and bacteria play critical roles in shaping marine ecosystems. However, the intricate relationships within these communities--particularly in extreme and rapidly changing environments like the coastal Southern Ocean--remain poorly understood. Here, we apply targeted methods to directly characterize the microbiomes of individual colonies of Phaeocystis antarctica, a keystone phytoplankton species in the Southern Ocean, for the first time. We show that colony microbiomes are consistent in distinct geographic locations at approximately the same time, but shift significantly after a year of laboratory culture. The bacterial orders Alteromonadales, Oceanospirillales, and Sphingomonadales dominated the microbiomes of all field-collected colonies, whereas Caulobacterales, Cellvibrionales, and Rhodobacterales dominated colony microbiomes after culturing. Notably, the most abundant genera in field-collected colony microbiomes, the psychrophiles Paraglaciecola and Colwellia, were lost in culture. The shift in microbiome structure emphasizes the importance of field-based studies to capture the complexity of microbial interactions, especially for species from polar environments that are difficult to replicate in laboratory conditions. Furthermore, the relative abundances of bacterial taxa comprising the majority of field-collected colony microbiomes--e.g., Paraglaciecola sp. (Alteromonadales) and Nitrincolaceae (Oceanospirillales)--were strongly associated with Phaeocystis abundance in surface waters, highlighting their potential roles in bloom dynamics and carbon cycling. This research provides valuable insights into the ecological significance of prokaryotic interactions with a key phytoplankton species and underscores the necessity of considering these dynamics in the context of climate-driven shifts in marine ecosystems.