Autecology of an oscillating population of a novel host-associated <i>Phaeobacter</i> species proliferating in marine bryozoans

<i>Phaeobacter</i> are marine alphaprotebacteria capable of producing a potent antibacterial compound, tropodithietic acid. Here we demonstrate that they are part of the microbiome of marine bryozoans where they during warmer months reach 10⁵ CFU/g. The levels exhibited a bimodal fluctuation, in both bryozoans and seawater across seasons. However, the population of <i>Phaeobacter</i> sp. was already established in the bryozoans prior to the peak in seawater and did not accumulate as a function of filter feeding on phytoplankton biomass, suggesting that the seawater population is likely seeded from the bryozoan-associated <i>Phaeobacter</i> sp. population rather than the opposite. By comparing whole-genome sequences of more than 100 bryozoan-associated <i>Phaeobacter</i> isolates sampled over a 12-year period, we found that all belonged to the same novel species and no systematic genetic changes occurred within it over the 12 year sampling period despite the fact that the population oscillated from below the limit of detection and across five orders of magnitude to 5.2 Log₁₀ CFU g^-1 bryozoan within individual years and hence were subject to drift. All isolates had the genetic capacity to produce tropodithietic acid (TDA) and the algicidal compounds, roseobacticides. The genes encoding the enzymes for TDA biosynthesis remained stable over time, indicating a conserved phenotype important in the ecophysiology of the bacteria. TDA biosynthetic genes were actively transcribed within the bryozoan host further corroborating the notion that the secondary metabolites of this novel host-associated <i>Phaeobacter</i> sp. may be central to its role within the bryozoan microbiome.