期刊名称:Proceedings of the National Academy of Sciences
印刷版ISSN:0027-8424
电子版ISSN:1091-6490
出版年度:2021
卷号:118
期号:33
DOI:10.1073/pnas.2107695118
语种:English
出版社:The National Academy of Sciences of the United States of America
摘要:Significance
Algae live in association with microbes that interact by a variety of chemical mediators, resulting in mutualistic or antagonistic relationships. Although algae are key contributors to carbon fixation and are fundamental for food webs, we still know little about the underlying molecular mechanisms affecting their fitness. This study investigates the interaction between an antagonistic bacterium and a unicellular alga. It demonstrates multiple roles of a polyyne, protegencin, that is used by the bacteria to attack green algal cells. It is a highly effective toxin that alters a subcellular algal compartment used for vision, bleaches, and lyses the algal cells. These results expand our knowledge of the arsenal of chemical mediators in bacteria and their modes of action in algal communities.
Algae are key contributors to global carbon fixation and form the basis of many food webs. In nature, their growth is often supported or suppressed by microorganisms. The bacterium
Pseudomonas protegens Pf-5 arrests the growth of the green unicellular alga
Chlamydomonas reinhardtii, deflagellates the alga by the cyclic lipopeptide orfamide A, and alters its morphology [P. Aiyar
et al.,
Nat. Commun. 8, 1756 (2017)]. Using a combination of Raman microspectroscopy, genome mining, and mutational analysis, we discovered a polyyne toxin, protegencin, which is secreted by
P. protegens, penetrates the algal cells, and causes destruction of the carotenoids of their primitive visual system, the eyespot. Together with secreted orfamide A, protegencin thus prevents the phototactic behavior of
C. reinhardtii. A mutant of
P. protegens deficient in protegencin production does not affect growth or eyespot carotenoids of
C. reinhardtii. Protegencin acts in a direct and destructive way by lysing and killing the algal cells. The toxic effect of protegencin is also observed in an eyeless mutant and with the colony-forming Chlorophyte alga
Gonium pectorale. These data reveal a two-pronged molecular strategy involving a cyclic lipopeptide and a conjugated tetrayne used by bacteria to attack select Chlamydomonad algae. In conjunction with the bloom-forming activity of several chlorophytes and the presence of the
protegencin gene cluster in over 50 different
Pseudomonas genomes [A. J. Mullins
et al., bioRxiv [Preprint] (2021).
https://www.biorxiv.org/content/10.1101/2021.03.05.433886v1 (Accessed 17 April 2021)], these data are highly relevant to ecological interactions between Chlorophyte algae and Pseudomonadales bacteria.