Chemical Signaling in Ecology and Evolution

 

I am generally interested in the chemical ecology of aquatic organisms. Currently, we are studying how small molecules biosynthesized by sea slugs (but potentially any abundant producer) may act as 'keystone molecules' with disproportionate impact on the surrounding communities and ecosystem. We are also studying the biosynthesis of polyketides in animals, following our discovery of a new family of enzymes (AFPKs) that make ecologically important small molecules in most highly diverse animal groups, and the coevolution of this pathway for secondary metabolites and photosynthesis in sacoglossans. Our lab is interested in how algal defenses influenced the diversification of Sacoglossa. Past work has looked at the chemical basis for habitat choice by larvae, sperm navigation, and foraging by scavengers - these could be topics for future student projects.

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1. Keystone molecules in estuarine ecology.

 

Students of ecology are familiar with keystone species, which have outsized effects relative to their abundance on their broader ecosystem. By extension, we are studying cases where low concentrations of keystone molecules may similarly have critical but overlooked roles in structuring marine communities. In wetlands, sea slugs in the genus Alderia are exceptionally abundant grazers, reaching peak densities of over 9,000 slugs per m2 on patches in California and in Europe. We recently characterized five small molecules in the class termed polyketides that make slugs unpalatable to predatory fish, crabs and worms. Moreover, these compounds also repel most infauna (microscopic animals living in the mud), causing crustaceans, worms and molluscs to leave the upper sediment. In contrast, snails preferentially lay their eggs where slug compounds are present, highlighting complex ecological interactions mediated by these small molecules. 

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We are continuing this work in ongoing projects by exploring possible mutualisms, cases of mimicry, and tracing the fate of slug biomass. With the Zellmer lab at Occidental College, we are working on species-distribution models to predict the occurrence of estuarine taxa like Alderia from environmental data, and to model how distributions may shift under climate change scenarios. I hope this will call attention to overlooked effects of chemical defenses in other systems; leaky defenses may often act as signals or have off-target influences and shadows that disrupt communities and ecosystems in unpredictable ways. 

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Scesa, P., Nguyen*, H., Weiss*, P., Rodriguez*, A., Garchow*, M. Ohlemacher, S.I., Prappas*, E., Caplins, S.A., Bewley, C.A., Bohnert, L., Zellmer, A.J., Wood, E., Schmidt, E.W. and P.J. Krug. Defensive polyketides produced by an abundant gastropod are candidate keystone molecules in estuarine ecology. Science Advances, 10, eadp8643.

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2. A new biosynthetic pathway for animal chemical defense

  

Most chemical defenses are broadly categorized in one of three groups of small molecules that can mediate ecological interactions. Alkaloids are nitrogen-containing compounds like tetradotoxin or nicotine that are usually derived from amino acids. Terpenes, like limonene from citrus, are made from 5-carbon building blocks; they are widespread in plants, sponges and corals, and are related to sterol metabolism. Polyketides are polymers of short carbon units, usually 2- or 3-carbon building blocks that are strung together, reduced, oxygenated and cyclized; this branch of secondary metabolism is related to fatty acid metabolism, but produces diverse metabolites including antibiotics (erythromycin), pigments (the purple of purple urchins, or green of parakeets), pheromones (bombykol from moths), and defensive molecules. There are canonical polyketide synthase (PKS) enzymes in every major branch of life.

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Working with Eric Schmidt's lab at the Univ. of Utah, we recently characterized a new family of polyketide-synthesizing enzymes. Surprisingly, these genes were closely related to fatty acid synthase enzymes from primary animal metabolism, but only distantly related to traditional animal PKSs. This new enzyme family, the animal fatty-acid-like polyketide synthases (AFPKs), is found in protostome invertebrates and makes small polyketides in sea slugs. Private AFPK lineage expansions have occurred in the three most species-rich animal groups: beetles, spiders, and heterobranch gastropods (sea slugs, traditional pulmonate snails and kin); hence the capacity to biosynthesize small molecules could be linked to evolutionary diversification. Prior work showed these enzymes (not recognized at the time as AFPKs) make insect cuticular hydrocarbon pheromones, so these genes could be highly important in maintaining species boundaries and in diverse other processes. However, their ecological functions and biochemistry are just starting to be explored.  

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Lin, Z., Li, F., Krug, P.J, and E.W. Schmidt. 2024. The polyketide to fatty acid transition in the evolution of animal lipid metabolism. Nature Communications, 15: 236.

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​​Li, F., Lin, Z., Krug, P.J, Catrow, J.L., Cox, J.E., and E.W. Schmidt. 2023. Animal FAS-like polyketide synthases produce diverse polypropionates. Proceedings of the National Academy of Sciences USA, 120: e2305575120.  (https://doi.org/10.1073/pnas.2305575120)

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3. Defensive traits vs consumer diversity

  

Using a phylogeny of over 400 species of sea slugs in clade Sacoglossa, we are using phylogenetic comparative methods to model how algal defensive traits like chemistry and calcification affect herbivore diversity, over both ecological and evolutionary timescales. 

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4. Habitat choice through chemical settlement cues

  

Most marine invertebrates spend their adult life on the sea floor. Dispersal, which permits gene flow between populations, is accomplished by tiny larvae that spend anywhere from minutes to months in the plankton. Eventually, larvae face the challenge of locating a suitable adult habitat before settling to the bottom. Finding a good area is critical for species that depend on one host or prey species; if the adult host is not found soon after the larva completes its metamorphosis, the juvenile will starve. We have studied how chemical cues mediate settlement in laboratory and field experiments. Research focused on larvae of the sea slug Alderia willowi, which settle in response to carbohydrates produced by the adult host alga Vaucheria. This work employed chemical techniques such as NMR and GC/MS to characterize bioactive oligosaccharides, and video motion analysis to quantify changes in larval swimming and settlement behavior in response to dissolved cues of habitat suitability. 

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Romero*, M.R., Phuong*, M., Bishop, C.D., and P.J. Krug. 2013. Differential function of nitric oxide signaling during habitat choice by two larval morphs of the sea slug Alderia willowi: mechanistic insight into evolutionary transitions in dispersal strategies. Journal of Experimental Biology, 216: 1114-1125.

(doi: 10.1242/jeb.080747) PDF

 

Botello*, G. and P.J. Krug. 2006. Desperate larvae revisited: Age, energy and experience affect sensitivity to settlement cues in larvae of the gastropod Alderia sp. Marine Ecology Progress Series 312: 149-159. PDF

 

Krug, P.J. 2006. “Defense of benthic invertebrates against surface colonization by larvae: A chemical arms race.”  Pp. 1-53 in: Clare A. and Fusetani N. (eds) Marine Molecular Biotechnology, vol 2. Springer, Berlin. PDF

 

Krug, P.J. and R.K. Zimmer. 2004. Developmental dimorphism: Consequences for larval behavior and dispersal potential in a marine gastropod.  Biological Bulletin 207: 233-246. PDF

 

Krug, P.J.  2001.  Bet-hedging dispersal strategy of a specialist marine herbivore: A settlement dimorphism among sibling larvae of Alderia modesta.  Marine Ecology Progress Series 213: 177-192. PDF

 

Krug, P.J. and R.K. Zimmer. 2000. Developmental dimorphism and expression of chemosensory-mediated behavior: Habitat selection by a specialist marine herbivore. Journal of Experimental Biology 203: 1741-1754. PDF

 

Krug, P.J. and R.K. Zimmer. 2000. Larval settlement: chemical markers for tracing production, transport, and distribution of a waterborne cue. Marine Ecology Progress Series 207: 283-296. PDF

 

Krug, P.J., and A.E. Manzi,  1999.  Waterborne and surface-associated carbohydrates as settlement cues for larvae of the specialist marine herbivore Alderia modesta.  Biological Bulletin 197: 94-103. PDF

 

Sperm navigation: sex and the single cell

 

From coral reefs to human beings, chemical communication between eggs and sperm plays a critical role in reproduction. Sperm cells can orient and accelerate towards an egg by tracking diffusing signal molecules, thereby enhancing fertilization success. This is especially important for broadcast-spawning organisms that shed their gametes into the sea, where they are rapidly diluted in the surrounding seawater. Species-specific sperm attractants may also function as pre-zygotic agents driving reproductive isolation and speciation, by allowing sperm to faithfully distinguish eggs of their own from related species. 

 

We identified the amino acid L-tryptophan as the sperm attractant from eggs of red abalone, a commercially valuable but endangered resource. Although such chemical signals might maintain species boundaries in these free-spawning animals, evidence indicates that soluble signals are less evolutionarily important that are rapidly evolving gamete recognition proteins. Ecologically, this work has implications for conservation, as low population densities of abalone may prevent appreciable fertilization from occurring due to gamete dilution. Improved understanding of chemical and biological mechanisms affecting reproductive success may thus aid management and restoration efforts for threatened species.

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Krug, P.J., Riffell, J., and R.K. Zimmer. 2009. Endogenous signaling pathways and chemical communication between sperm and egg. Journal of Experimental Biology, 212: 1092-1100. PDF

 

Riffell, J., Krug, P.J., and R.K. Zimmer. 2004. The ecological and evolutionary consequences of sperm chemoattraction.  Proceedings of the National Academy of Sciences USA 101: 4501-4506. PDF

 

Riffell, J., Krug, P.J., and R.K. Zimmer. 2002. Fertilization in the sea: The chemical identity of an abalone sperm attractant. Journal of Experimental Biology 205: 1439-1450. [Cover article] PDF​