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Marine eggs and embryos, the very epitome of vulnerability, tossed hither and yon like so much flotsam and jetsam in those vast bodies of water, not to mention the teeming multitude of visible and invisible predators. How could they ever emerge alive? Sounds like a dicey predicament to say the least. Yet through ingenious adaptive processes that are surprisingly robust and resilient, marine eggs and embryos successfully yield new life generation after generation. Marine organisms that birth their live outside their body use two main strategies to protect potential future offspring from disease agents, Trans-generational Immune Priming (TGIP) and Transmission of symbiotic partners, partners that include microbes and eukaryotes, and transmission that’s either vertical (mother-to-egg) or horizontal (parental environment-to-egg).

TGIP (Trans-generational Immune Priming)

  • Quite the unwieldy mouthful, TGIP is similar to Passive Immunity. In humans, Passive Immunity largely consists of mother-to-child transfer of antibodies, in utero and through breast milk.
  • Most marine organisms are invertebrates and lack the capacity to make antibodies. Instead, the mother’s immune experience is transferred to its eggs in the form of other immune factors. Ranging from enzymes to sugars to microbe-binding proteins to inhibitors, they cover the gamut of biological molecules and effector functions.
  • The process also illustrates the laser-like efficiency of nature’s parsimony. Eggs and embryos take a tremendous amount of energy, a perilous undertaking in the best of times given that nature doesn’t guarantee food security. To do so outside the body, as happens in many marine organisms, makes it fraught with even more peril. In such a situation, making a variety of immune responses is an undue, even untenable burden on vulnerable eggs and embryos.
  • Maternal transfer of her immune experience is a brilliant solution. It not only spares eggs the excessive burden of making immune responses from scratch but by transferring factors that successfully deterred pathogens the mother herself encountered, it’s a transfer of precisely the ones likely most needed by eggs. Two essential literally life-saving functions fulfilled in one fell swoop. Research thus reveals that trans-generational transfer of immunological experience is no longer the purview of the so-called ‘higher‘ animals alone.

Transmission of symbiotic partners, vertical (mother-to-egg) or horizontal (peer-to-peer or environment-to-egg)

  • A holobiont is a host organism plus its symbiotic partners, typically but not only micro-organisms.
  • Symbiont transmission from one generation to the next, either vertically or horizontally, is essential for holobiont maintenance (1; see figure below).
  • Vertical, i.e., directly from parent to offspring, and horizontal, i.e., indirectly through the environment. Examples of both modes together also exist.
  • Vertical transmission has immense benefit for the symbiotic partner since it’s guaranteed a new host body with each successive generation. Yet there’s also heart-stopping cost to hitching one’s wagon so firmly to just that one partner. In the partner’s extinction lies one’s own.
  • Horizontal transmission does not tie the mutually dependent bond quite so tight but reduces the chances of partners unerringly finding each other generation after generation.
  • As is the case with nature, each mode accentuates the tenuousness of such biological relationships, which only serves to enhance the exhilaration that comes from knowing they have withstood the test of evolutionary time.

Some examples of TGIP (Trans-generational Immune Priming)

  • Scallop are Bivalvia. Their eggs are externally fertilized in seawater.
  • One study found maternal-to-egg transfer of anti-microbial proteins that were very potent against gram-negative bacteria such as E. coli and Vibrio anguillarum, and fungi such as Pichia pastoris, causing them to agglutinate as well as killing them (2).

Cephalopods (cuttlefish, octopus, squid)

  • In coastal waters, adult females release fertilized eggs that then have to fend for themselves for >2 months. Yolk provides necessary nutrients. What about protection?
  • Obvious question too long ignored, only in 2015 were anti-microbial factors identified in the cuttle fish, Sepia officinalis.
  • Produced in the female’s genital nidamental glands and carefully secreted into and on eggshells, they’re an unmistakable sign of assiduous parental investment in their future offsprings’ defense (3, 4).

Molluscs including gastropods

  • In spectacularly colorful fashion, one mollusc eats its way to trans-generational anti-microbial defense.
  • The ‘Spanish dancer‘ is a dazzlingly colorful example of dietary anti-microbial defense. A large nudibranch mollusc, Hexabranchus sanguineus, the ‘Spanish dancer’ lives among coral reefs all over the Indo-Pacific region (5).
  • As Pawlik et al write, ‘It is renowned for its spectacular swimming response, wherein the slug throws its body into sweeping dorsoventral flexions, sending synchronous unduIations through the broad and vividly patterned red and white margins of its mantle. This display has earned it the common name ‘Spanish dancer‘ (6).
  • This mollusc derives potent anti-microbials from specific sponges that it eats and indiscriminately strews its eggs, colored bright pink to red and called ‘egg ribbons‘, as coiled rosettes (see figure below) among rocks and corals (5).
  • These anti-microbials, specifically Macrolide, are >10X more concentrated in the ‘egg ribbons‘ and are powerful anti-fungals (6). Accident? Unlikely.


  • Several studies show that mollusc eggs contain other potent anti-microbial compounds (7, 8, 9, 10, 11).
    • These include factors that agglutinate bacteria and bind viruses (12; see table below).
    • More recent studies are more relevant. Instead of testing potency against generic microbes or against human disease-specific microbes, they tested and showed activity against marine microbes, especially against those that form biofilms on molluscs (13).


  • The gastropod Dicathais orbita incorporates several strategies against microbial attack (14).
    • The egg shell surface discourages bacterial attachment.
    • It sheds the outer layer which removes any microbes that may have colonized it.
    • It secretes as-yet-uncharacterized chemicals that repel bacterial growth.

Digressing just a bit, this table of approved (for humans) drugs originally discovered in marine organisms allays any doubt whatsoever of their capacity to be a veritable cornucopia of pharmacopoeia (sorry, couldn’t resist such a delicious alliteration) (15).

Some examples of symbiont transmission, vertical and horizontal
Molluscs including gastropods

  • The gastropod Concholepas concholepas vertically transmits Bacillus species bacteria to its eggs. Located in the egg capsule, these bacteria inhibit the pathogenic bacterium, Vibrio parahaemolyticus (16).
  • In an even more spectacular example, not only is there vertical transmission of a specific bacterium from the mollusc, Argopecten purpuratus, to its eggs, the bacterium gets into the intestine of the ensuing larvae and protects against pathogens during larval development (17).


  • Specializing in vertical transmission of their symbiotic microbial partners, sponges have also chosen to literally put all their eggs in one basket in more ways than one.
  • Archaea, bacteria, yeast, the specific microorganisms associated with sponges, sponge-specific microorganisms, or with sponges and corals, sponge and coral-specific microorganisms, are faithfully transmitted from parents to eggs through vertical transmission (18).


  • Corals either brood or spawn eggs.
    • Former? Sperm are released but eggs retained inside. Fertilized eggs kept and developed inside gastrovascular cavities of polyps whence planula larvae are released.
    • Latter? Large numbers of eggs and sperm released into water where fertilization and development occurs.
  • The algae Symbiodinium is an important coral symbiont.
    • Brooding coral mothers vertically transmit it to their larvae (19, 20).
    • Some spawning coral mothers can also vertically transmit it by seeding their eggs with it (21, 22, 23).
    • Other spawning corals horizontally transmit it when externally fertilized larvae acquire it from the environment (24, 25).
  • Roseobacter species have emerged as important bacterial symbionts of corals (26).
    • Horizontally transmitted in the coral, Pocillopora meandrina (21) and seven other species (27).
    • Both types of corals (brooding or spawning) release bacteria when they spawn. These are largely Roseobacter and Alteromonas species (28).
    • In spawning corals, the process is simply marvelous. Released as bundles, gametes’ mucus coats contain bacterial populations similar to those in their parental colonies.
    • Either the mother corals seed the egg mucus coats prior to spawning (vertical transmission) or after spawning, parents release their microbial symbionts into the seawater and onto the spawned eggs (horizontal transmission) (21, 22, 28, 29). See figure below from 30.
  • Corals are thus a literal example of the proverb, ‘it takes a village (to raise a child)‘ (It takes a village).
  • How do these symbionts help protect coral spawns or larvae?
    • Studies in adult corals suggest symbionts are likely source of anti-microbial peptides and inhibitors of pathogenic microbial colonization (30, 31).
    • Given that symbionts are transmitted to successive generations in every phylum, it’s no longer too much of a stretch to call trans-generational transmission of symbiotic partners a fundamental attribute in biology (1).


Cephalopods (cuttlefish, octopus, squid)

  • I’ve written about the exquisite squid-bacterium lifelong celestial dance-like co-op in more detail elsewhere*.
  • The partners are Euprymna scolopes, the Hawaiian bobtail squid and Vibrio fischerii.
  • Here, let’s focus on the vertical transmission of squids’ symbiotic partners in general.
  • Squid females have an accessory nidamental gland (ANG).
    • It makes the jelly that coats the squid eggs.
    • The gland consists of tubules lined with epithelium that support dense populations of different bacterial species, largely of the Roseobacter clade.
    • So the squid mother doesn’t just squirt jelly onto her newly laid eggs.
    • Rather she’s also fulfilling her evolutionary mandate of transmitting to her progeny the symbiotic microbial partners that sustained her in health through the course of her life (32, 33, 34, 35, 36, 37, 38, 39, 40).
  • Exactly how do symbionts mediate marine egg/embryo anti-pathogen defense? Research on this is in its infancy. It’s amply clear though that marine organisms meticulously transmit their symbiont partners to their eggs/embryos.


  1. Rosenberg, Eugene, and Ilana Zilber-Rosenberg. “Microbiotas are transmitted between holobiont generations.” The Hologenome Concept: Human, Animal and Plant Microbiota. Springer International Publishing, 2013. 41-54.
  2. Yue, Feng, et al. “Maternal transfer of immunity in scallop Chlamys farreri and its trans-generational immune protection to offspring against bacterial challenge.” Developmental & Comparative Immunology 41.4 (2013): 569-577.
  3. Matozzo, Valerio, et al. “A first survey on the biochemical composition of egg yolk and lysozyme-like activity of egg envelopment in the cuttlefish Sepia officinalis from the Northern Adriatic Sea (Italy).” Fish & shellfish immunology 45.2 (2015): 528-533.
  4. Cornet, Valérie, et al. “How Egg Case Proteins Can Protect Cuttlefish Offspring?.” PloS one 10.7 (2015): e0132836. http://www.plosone.org/article/f…
  5. Gohar, H. A. F., and G. N. Soliman. “The biology and development of Hexabranchus sanguineus (Rüpp. and Leuck.)(Gastropoda, Nudibranchiata).” Publ Mar Biol Sta Ghardaqa (Red Sea) 12 (1963): 219-247.
  6. Pawlik, Joseph R., et al. “Defensive chemicals of the Spanisch dancer nudibranch Hexabranchus sanguineus and its egg ribbons: macrolides derived from a sponge diet.” Journal of Experimental Marine Biology and Ecology 119.2 (1988): 99-109. http://people.uncw.edu/pawlikj/1…
  7. Benkendorff, Kirsten, Andrew R. Davis, and John B. Bremner. “Chemical defense in the egg masses of benthic invertebrates: an assessment of antibacterial activity in 39 mollusks and 4 polychaetes.” Journal of invertebrate pathology 78.2 (2001): 109-118. Page on researchgate.net
  8. Benkendorff, Kirsten, Ramesh Pillai, and John B. Bremner. “2, 4, 5-Tribromo-1 H-Imidazole in the egg masses of three muricid molluscs.” Natural product research 18.5 (2004): 427-431. Page on researchgate.net
  9. Benkendorff, Kirsten, et al. “Free fatty acids and sterols in the benthic spawn of aquatic molluscs, and their associated antimicrobial properties.” Journal of Experimental Marine Biology and Ecology 316.1 (2005): 29-44. Page on scu.edu.au
  10. Ramasamy, M. Santhana, and A. Murugan. “Fouling deterrent chemical defence in three muricid gastropod egg masses from the Southeast coast of India.” Biofouling 23.4 (2007): 259-265.
  11. Hathaway, Jennifer JM, et al. “Identification of protein components of egg masses indicates parental investment in immunoprotection of offspring by Biomphalaria glabrata (Gastropoda, Mollusca).” Developmental & Comparative Immunology 34.4 (2010): 425-435. Page on nih.gov
  12. Wang, Lingling, et al. “Maternal immune transfer in mollusc.” Developmental & Comparative Immunology 48.2 (2015): 354-359.
  13. Ramasamy, M. Santhana, and A. Murugan. “Potential antimicrobial activity of marine molluscs from tuticorin, southeast coast of India against 40 biofilm bacteria.” Journal of Shellfish Research 24.1 (2005): 243-251.
  14. Lim, Norman SH, et al. “Comparison of surface microfouling and bacterial attachment on the egg capsules of two molluscan species representing Cephalopoda and Neogastropoda.” Aquatic microbial ecology 47.3 (2007): 275. Page on scu.edu.au
  15. Ng, Tzi Bun, et al. “Antibacterial products of marine organisms.” Applied microbiology and biotechnology 99.10 (2015): 4145-4173.
  16. Leyton, Yanett, and Carlos Riquelme. “Marine Bacillus spp. Associated with the egg capsule of Concholepas concholepas (common name “loco”) have an inhibitory activity toward the pathogen Vibrio parahaemolyticus.” Microbial ecology 60.3 (2010): 599-605.
  17. Riquelme, C., et al. “Evidence for parental bacterial transfer to larvae in Argopecten purpuratus (Lamarck, 1819).” Biological Research 27 (1994): 129-134.
  18. Sipkema, Detmer, et al. “Similar sponge‐associated bacteria can be acquired via both vertical and horizontal transmission.” Environmental microbiology (2015).
  19. Maruyama, Tadashi, et al. “Molecular phylogeny of zooxanthellate bivalves.” The Biological Bulletin 195.1 (1998): 70-77. Page on biolbull.org
  20. Baker, Andrew C. “Flexibility and specificity in coral-algal symbiosis: diversity, ecology, and biogeography of Symbiodinium.” Annual Review of Ecology, Evolution, and Systematics (2003): 661-689. Page on wwu.edu
  21. Apprill, Amy, et al. “The onset of microbial associations in the coral Pocillopora meandrina.” The ISME journal 3.6 (2009): 685-699. Page on nature.com
  22. Sharp, Koty H., Dan Distel, and Valerie J. Paul. “Diversity and dynamics of bacterial communities in early life stages of the Caribbean coral Porites astreoides.” The ISME journal 6.4 (2012): 790-801.
  23. Padilla-Gamiño, Jacqueline L., et al. “From parent to gamete: vertical transmission of Symbiodinium (Dinophyceae) ITS2 sequence assemblages in the reef building coral Montipora capitata.” (2012): e38440. Page on plosone.org
  24. Baker, Andrew C. “Flexibility and specificity in coral-algal symbiosis: diversity, ecology, and biogeography of Symbiodinium.” Annual Review of Ecology, Evolution, and Systematics (2003): 661-689. Page on wwu.edu
  25. Trench, ROBERT K. “Dinoflagellates in non-parasitic symbioses.” The biology of dinoflagellates (1987): 530-570.).
  26. Lema, Kimberley A., David G. Bourne, and Bette L. Willis. “Onset and establishment of diazotrophs and other bacterial associates in the early life history stages of the coral Acropora millepora.” Molecular ecology 23.19 (2014): 4682-4695.
  27. Sharp, Koty H., et al. “Bacterial acquisition in juveniles of several broadcast spawning coral species.” PloS one 5.5 (2010): e10898. Page on plosone.org
  28. Ceh, Janja, Mike van Keulen, and David G. Bourne. “Intergenerational transfer of specific bacteria in corals and possible implications for offspring fitness.” Microbial ecology 65.1 (2013): 227-231.
  29. Kirk, Nathan L., et al. “Tracking transmission of apicomplexan symbionts in diverse Caribbean corals.” (2013): e80618. Page on plosone.org
  30. Thompson, Janelle R., et al. “Microbes in the coral holobiont: partners through evolution, development, and ecological interactions.” Frontiers in cellular and infection microbiology 4 (2014).
  31. Nissimov, Jozef, Eugene Rosenberg, and Colin B. Munn. “Antimicrobial properties of resident coral mucus bacteria of Oculina patagonica.” FEMS microbiology letters 292.2 (2009): 210-215. Antimicrobial properties of resident coral mucus bacteria of Oculina patagonica
  32. Bloodgood, Robert A. “The squid accessory nidamental gland: ultrastructure and association with bacteria.” Tissue and Cell 9.2 (1977): 197-208.
  33. Lum‐Kong, A., and T. S. Hastings. “The accessory nidamental glands of Loligo forbesi (Cephalopoda: Loliginidae): characterization of symbiotic bacteria and preliminary experiments to investigate factors controlling sexual maturation.” Journal of Zoology 228.3 (1992): 395-403.
  34. Barbieri, Elena, et al. “Antimicrobial activity in the microbial community of the accessory nidamental gland and egg cases of Loligo pealei (Cephalopoda: Loliginidae).” The Biological Bulletin 193.2 (1997): 275. Antimicrobial Activity in the Microbial Community of the Accessory Nidamental Gland and Egg Cases of Loligo pealei (Cephalopoda: Loliginidae)
  35. Kaufman, Melissa R., et al. “Bacterial symbionts colonize the accessory nidamental gland of the squid Loligo opalescens via horizontal transmission.” The Biological Bulletin 194.1 (1998): 36-43. http://www.biolbull.org/content/…
  36. Grigioni, S., et al. “Phylogenetic characterisation of bacterial symbionts in the accessory nidamental glands of the sepioid Sepia officinalis (Cephalopoda: Decapoda).” Marine Biology 136.2 (2000): 217-222
  37. Barbieri, Elena, et al. “Phylogenetic characterization of epibiotic bacteria in the accessory nidamental gland and egg capsules of the squid Loligo pealei (Cephalopoda: Loliginidae).” Environmental microbiology 3.3 (2001): 151-167
  38. Pichon, Delphine, et al. “Phylogenetic diversity of epibiotic bacteria in the accessory nidamental glands of squids (Cephalopoda: Loliginidae and Idiosepiidae).” Marine Biology 147.6 (2005): 1323-1332. Page on anu.edu.au
  39. Nair, P., and P. M. Sherief. “Antibacterial activity in the accessory nidamental gland extracts of the Indian squid, Loligo duvauceli Orbigny.” Indian J. Mar. Sci 39 (2010): 100-104. Page on niscair.res.in
  40. Collins, Andrew J., et al. “Diversity and partitioning of bacterial populations within the accessory nidamental gland of the squid Euprymna scolopes.” Applied and environmental microbiology 78.12 (2012): 4200-4208. Diversity and Partitioning of Bacterial Populations within the Accessory Nidamental Gland of the Squid Euprymna scolopes

*Tirumalai Kamala’s answer to What are the most interesting examples of group behavior in bacteria?