In an early branching metazoan, bacterial colonization of the embryo is controlled by maternal antimicrobial peptides

Abstract

Early embryos of many organisms develop outside the mother and are immediately confronted with myriads of potential colonizers. How these naive developmental stages control and shape the bacterial colonization is largely unknown. Here we show that early embryonic stages of the basal metazoan Hydra are able to control bacterial colonization by using maternal antimicrobial peptides. Antimicrobial peptides of the periculin family selecting for a specific bacterial colonization during embryogenesis are produced in the oocyte and in early embryos. If overexpressed in hydra ectodermal epithelial cells, periculin1a drastically reduces the bacterial load, indicating potent antimicrobial activity. Unexpectedly, transgenic polyps also revealed that periculin, in addition to bactericidal activity, changes the structure of the bacterial community. These findings delineate a role for antimicrobial peptides both in selecting particular bacterial partners during development and as important components of a "be prepared" strategy providing transgenerational protection.innate immunity | host-microbe interaction | embryo protection | cnidaria | Hydra

Naturally occurring tumours in the basal metazoan Hydra

“…1e-h). Although periculin expression is activated not only during oogenesis but also by a number of environmental signals 23 , the observation of tumour cells expressing both Cnnos1 and periculin supports the view that tumour cells are committed to the female germline. A quantitative morphological analysis showed that the cells within tumours are predominantly large ISCs 19 (Fig.…”

“…This polyclonal antibody that was raised against periculin1a in Hydra vulgaris recognizes multiple paralogues of periculin 23 . This property of the antipericulin antibody, the presence of at least four periculin paralogues in H. oligactis and possible expression of some of the periculin paralogues outside the context of female germline preclude any firm conclusion about cellular origin of the tumour cells.…”

“…Immunohistochemical detection of periculin protein in whole mount Hydra preparations was performed as described previously 23 using polyclonal mouse antisera against periculin1a protein (1:500 diluted, produced by T. Bosch lab) and Alexa488-conjugated donkey-anti-mouse secondary antibodies (2 mg ml À 1 ; Invitrogen, Eugene, OR, USA). Rhodamin-phalloidin and TO-PRO3 counterstaining was conducted as described previously 34 .…”

“…3). Immunocytochemistry with an antibody against periculin protein, known to label Hydra's female germline precursor cells 23 , revealed that in both lines the interstitial cells in the tumour tissue are expressing this female-specific marker ( Fig. 2d and Supplementary Fig.…”

Distinct antimicrobial peptide expression determines host species-specific bacterial associations

“…Studies in mice have shown that the expression level of AMPs of the α-defensin family greatly affects community composition (25). In the cnidarian Hydra, sequentially expressed AMPs of the periculin family mediate the establishment of the bacterial microbiota during embryogenesis (27).…”