Particle attachment drives seasonal abundance and photoheterotrophy of marine aerobic anoxygenic phototrophs

BackgroundAerobic Anoxygenic Phototrophic (AAP) bacteria are an essential component of aquatic microbial communities and play an important role in carbon cycling due to their ability to supplement their chemoorganotrophic metabolism with light-derived energy. While most of the previous studies focused on abundance, species composition and seasonal changes of AAP bacteria, their affinity for the particle-attachment did not attract much attention. Similarly, it remains unclear whether the entire AAP community is phototrophically active. This study investigated the seasonal changes in the composition of free-living and particle-attached AAP bacteria in the central Adriatic Seas coastal waters using both DNA and RNA pufM amplicon gene sequencing in the particle-attached and the free-living fractions. ResultsAAP bacterial abundance grew from 1.27 x 104 cells mL-1 in winter to 8.30 x 104 cells mL-1 in summer. The proportion of AAP bacteria was consistently higher in the particle-attached fraction, particularly in spring and summer. DNA and RNA pufM amplicon analyses revealed large differences in activity among the species forming the AAP communities. Additionally, DNA-based assessments underestimated the phototrophic activity of certain genera, demonstrating discrepancies between the gene presence and its functional activity. ConclusionsOur data demonstrated that the expression of phototrophic genes in AAP bacteria is not uniform and largely varies throughout seasons and fractions. The particle-attached fraction harboured more than twice as many active AAP bacteria as the free-living fraction, with seasonal shifts and lifestyle driving changes in the phototrophy gene expression. RNA and DNA libraries revealed discrepancies between total and active AAP bacterial communities, emphasizing the necessity of transcript-based approaches for accurately assessing photoheterotrophic activity in marine environments. The pronounced partitioning of AAP bacterial diversity and activity between free-living and particle-attached fractions indicated the ecological specialization of certain AAP lineages, which may have noteworthy implications for the consumption of particulate organic matter and, ultimately, carbon cycling in coastal waters.