Responses of the coastal bacterial community to viral infection of the algae Phaeocystis globosa

• Published in: The ISME Journal 2014-01, Vol.8 (1), p.212-225
• Main Authors: Sheik, Abdul R, Brussaard, Corina P D, Lavik, Gaute, Lam, Phyllis, Musat, Niculina, Krupke, Andreas, Littmann, Sten, Strous, Marc, Kuypers, Marcel M M
• Format: Article
• Language: English
• Subjects: 631/326/2565/855; Aggregates; Algae; Alteromonas; Bacteria; Bacterial Physiological Phenomena; Biodiversity; Biomass; Biomedical and Life Sciences; Carbon; Carbon - metabolism; Carbon Isotopes - metabolism; Chemical analysis; Community composition; Dissolved inorganic carbon; Ecology; Evolutionary Biology; Excretion; Haptophyta - microbiology; Haptophyta - virology; Life Sciences; Marine environment; Mass spectrometry; Microbial Ecology; Microbial Genetics and Genomics; Microbiology; Niches; Nitrogen - metabolism; Nitrogen Isotopes - metabolism; North Sea; Organic carbon; Organic matter; Original; original-article; Phaeocystis globosa; Proteobacteria - genetics; Proteobacteria - growth & development; Proteobacteria - physiology; RNA, Ribosomal, 16S - genetics; Seawater; Seawater - microbiology; Virus Physiological Phenomena; Water analysis
• ISSN: 1751-7362; 1751-7370
• DOI: 10.1038/ismej.2013.135

The release of organic material upon algal cell lyses has a key role in structuring bacterial communities and affects the cycling of biolimiting elements in the marine environment. Here we show that already before cell lysis the leakage or excretion of organic matter by infected yet intact algal cells shaped North Sea bacterial community composition and enhanced bacterial substrate assimilation. Infected algal cultures of Phaeocystis globosa grown in coastal North Sea water contained gamma- and alphaproteobacterial phylotypes that were distinct from those in the non-infected control cultures 5 h after infection. The gammaproteobacterial population at this time mainly consisted of Alteromonas sp. cells that were attached to the infected but still intact host cells. Nano-scale secondary-ion mass spectrometry (nanoSIMS) showed ∼20% transfer of organic matter derived from the infected 13 C- and 15 N-labelled P. globosa cells to Alteromonas sp. cells. Subsequent, viral lysis of P. globosa resulted in the formation of aggregates that were densely colonised by bacteria. Aggregate dissolution was observed after 2 days, which we attribute to bacteriophage-induced lysis of the attached bacteria. Isotope mass spectrometry analysis showed that 40% of the particulate 13 C-organic carbon from the infected P. globosa culture was remineralized to dissolved inorganic carbon after 7 days. These findings reveal a novel role of viruses in the leakage or excretion of algal biomass upon infection, which provides an additional ecological niche for specific bacterial populations and potentially redirects carbon availability.