Editors' ChoiceDevelopmental Biology

How bacteria induce animal metamorphosis

Sci. Signal.  13 Sep 2016:
Vol. 9, Issue 445, pp. ec211
DOI: 10.1126/scisignal.aaj1824

Some bacteria can release factors that induce the metamorphosis of marine invertebrates from the larval swimming form to the sessile juvenile form, and animals from diverse taxonomic groups depend on such interspecies signaling cues for normal developmental transitions. One such bacterial factor is called the metamorphosis-associated contractile structures (MACs), which are produced by Pseudoalteromonas luteoviolacea, bacteria that induce the metamorphosis of the tubeworm Hydroides elegans. Shikuma et al. studied both sides of this interaction using MACs produced by two different bacterial mutants and by pharmacologically inhibiting the tubeworm’s mitogen-activated protein kinase (MAPK) signaling pathways. MACs are structurally complex arrays of phage tail–like structures similar to bacteriocins. Exposure to MACs extracted from mutant bacteria that could not produce a key structural component failed to induce even larval settlement onto a surface, the first step necessary before metamorphosis begins. Another bacterial mutant, which lacked a locus containing six uncharacterized protein-coding genes, produced MACs of apparently similar size and structure as the wild-type. Addition of this mutant MAC extract stimulated larval settlement but failed to induce further metamorphosis. Transcriptomic comparisons showed that worms exposed to wild-type MACs had increased expression of genes encoding proteins involved in innate immunity (kazal-type serine protease inhibitor domain–containing proteins) and tissue remodeling (matrix metalloproteinase and collagen triple helix–containing proteins). Expression of several genes involved in MAPK signaling pathways was also increased. Indeed, chemically inhibiting components of the p38 or c-Jun N-terminal kinase (JNK) MAPK signaling pathways blocked MAC-induced metamorphosis. These results identify molecular mechanisms involved in interspecies communication, which is critical for management of marine ecosystems and may help develop methods to prevent the attachment of marine organisms to ships.

N. J. Shikuma, I. Antoshechkin, J. M. Medeiros, M. Pilhofer, D. K. Newman, Stepwise metamorphosis of the tubeworm Hydroides elegans is mediated by a bacterial inducer and MAPK signaling. Proc. Natl. Acad. Sci. U.S.A. 113, 10097–10102 (2016). [PubMed]