The genomic and cellular basis of biosynthetic innovation in rove beetles

Sheila A. Kitchen; Thomas H. Naragon; Adrian Brückner; Mark S. Ladinsky; Sofia A. Quinodoz; Jean M. Badroos; Joani W. Viliunas; Yuriko Kishi; Julian M. Wagner; David R. Miller; Mina Yousefelahiyeh; Igor A. Antoshechkin; K. Taro Eldredge; Stacy Pirro; Mitchell Guttman; Steven R. Davis; Matthew L. Aardema; Joseph Parker

doi:10.1016/j.cell.2024.05.012

The genomic and cellular basis of biosynthetic innovation in rove beetles

Sheila A. Kitchen, Thomas H. Naragon, Adrian Brückner, Mark S. Ladinsky, Sofia A. Quinodoz, Jean M. Badroos, Joani W. Viliunas, Yuriko Kishi, Julian M. Wagner, David R. Miller, Mina Yousefelahiyeh, Igor A. Antoshechkin, K. Taro Eldredge, Stacy Pirro, Mitchell Guttman, Steven R. Davis, Matthew L. Aardema, Joseph Parker

Biology

Research output: Contribution to journal › Article › peer-review

3 Scopus citations

Abstract

How evolution at the cellular level potentiates macroevolutionary change is central to understanding biological diversification. The >66,000 rove beetle species (Staphylinidae) form the largest metazoan family. Combining genomic and cell type transcriptomic insights spanning the largest clade, Aleocharinae, we retrace evolution of two cell types comprising a defensive gland—a putative catalyst behind staphylinid megadiversity. We identify molecular evolutionary steps leading to benzoquinone production by one cell type via a mechanism convergent with plant toxin release systems, and synthesis by the second cell type of a solvent that weaponizes the total secretion. This cooperative system has been conserved since the Early Cretaceous as Aleocharinae radiated into tens of thousands of lineages. Reprogramming each cell type yielded biochemical novelties enabling ecological specialization—most dramatically in symbionts that infiltrate social insect colonies via host-manipulating secretions. Our findings uncover cell type evolutionary processes underlying the origin and evolvability of a beetle chemical innovation.

Original language	English
Pages (from-to)	3563-3584.e26
Journal	Cell
Volume	187
Issue number	14
DOIs	https://doi.org/10.1016/j.cell.2024.05.012
State	Published - 11 Jul 2024

Keywords

beetles
biosynthesis
cell type evolution
Dalotia
gene expression programs
genomics
key innovations
Staphylinidae

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10.1016/j.cell.2024.05.012

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Kitchen, S. A., Naragon, T. H., Brückner, A., Ladinsky, M. S., Quinodoz, S. A., Badroos, J. M., Viliunas, J. W., Kishi, Y., Wagner, J. M., Miller, D. R., Yousefelahiyeh, M., Antoshechkin, I. A., Eldredge, K. T., Pirro, S., Guttman, M., Davis, S. R., Aardema, M. L., & Parker, J. (2024). The genomic and cellular basis of biosynthetic innovation in rove beetles. Cell, 187(14), 3563-3584.e26. https://doi.org/10.1016/j.cell.2024.05.012

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title = "The genomic and cellular basis of biosynthetic innovation in rove beetles",

abstract = "How evolution at the cellular level potentiates macroevolutionary change is central to understanding biological diversification. The >66,000 rove beetle species (Staphylinidae) form the largest metazoan family. Combining genomic and cell type transcriptomic insights spanning the largest clade, Aleocharinae, we retrace evolution of two cell types comprising a defensive gland—a putative catalyst behind staphylinid megadiversity. We identify molecular evolutionary steps leading to benzoquinone production by one cell type via a mechanism convergent with plant toxin release systems, and synthesis by the second cell type of a solvent that weaponizes the total secretion. This cooperative system has been conserved since the Early Cretaceous as Aleocharinae radiated into tens of thousands of lineages. Reprogramming each cell type yielded biochemical novelties enabling ecological specialization—most dramatically in symbionts that infiltrate social insect colonies via host-manipulating secretions. Our findings uncover cell type evolutionary processes underlying the origin and evolvability of a beetle chemical innovation.",

keywords = "beetles, biosynthesis, cell type evolution, Dalotia, gene expression programs, genomics, key innovations, Staphylinidae",

author = "Kitchen, {Sheila A.} and Naragon, {Thomas H.} and Adrian Br{\"u}ckner and Ladinsky, {Mark S.} and Quinodoz, {Sofia A.} and Badroos, {Jean M.} and Viliunas, {Joani W.} and Yuriko Kishi and Wagner, {Julian M.} and Miller, {David R.} and Mina Yousefelahiyeh and Antoshechkin, {Igor A.} and Eldredge, {K. Taro} and Stacy Pirro and Mitchell Guttman and Davis, {Steven R.} and Aardema, {Matthew L.} and Joseph Parker",

note = "Publisher Copyright: {\textcopyright} 2024 Elsevier Inc.",

year = "2024",

month = jul,

day = "11",

doi = "10.1016/j.cell.2024.05.012",

language = "English",

volume = "187",

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Kitchen, SA, Naragon, TH, Brückner, A, Ladinsky, MS, Quinodoz, SA, Badroos, JM, Viliunas, JW, Kishi, Y, Wagner, JM, Miller, DR, Yousefelahiyeh, M, Antoshechkin, IA, Eldredge, KT, Pirro, S, Guttman, M, Davis, SR, Aardema, ML & Parker, J 2024, 'The genomic and cellular basis of biosynthetic innovation in rove beetles', Cell, vol. 187, no. 14, pp. 3563-3584.e26. https://doi.org/10.1016/j.cell.2024.05.012

TY - JOUR

T1 - The genomic and cellular basis of biosynthetic innovation in rove beetles

AU - Kitchen, Sheila A.

AU - Naragon, Thomas H.

AU - Brückner, Adrian

AU - Ladinsky, Mark S.

AU - Quinodoz, Sofia A.

AU - Badroos, Jean M.

AU - Viliunas, Joani W.

AU - Kishi, Yuriko

AU - Wagner, Julian M.

AU - Miller, David R.

AU - Yousefelahiyeh, Mina

AU - Antoshechkin, Igor A.

AU - Eldredge, K. Taro

AU - Pirro, Stacy

AU - Guttman, Mitchell

AU - Davis, Steven R.

AU - Aardema, Matthew L.

AU - Parker, Joseph

PY - 2024/7/11

Y1 - 2024/7/11

N2 - How evolution at the cellular level potentiates macroevolutionary change is central to understanding biological diversification. The >66,000 rove beetle species (Staphylinidae) form the largest metazoan family. Combining genomic and cell type transcriptomic insights spanning the largest clade, Aleocharinae, we retrace evolution of two cell types comprising a defensive gland—a putative catalyst behind staphylinid megadiversity. We identify molecular evolutionary steps leading to benzoquinone production by one cell type via a mechanism convergent with plant toxin release systems, and synthesis by the second cell type of a solvent that weaponizes the total secretion. This cooperative system has been conserved since the Early Cretaceous as Aleocharinae radiated into tens of thousands of lineages. Reprogramming each cell type yielded biochemical novelties enabling ecological specialization—most dramatically in symbionts that infiltrate social insect colonies via host-manipulating secretions. Our findings uncover cell type evolutionary processes underlying the origin and evolvability of a beetle chemical innovation.

AB - How evolution at the cellular level potentiates macroevolutionary change is central to understanding biological diversification. The >66,000 rove beetle species (Staphylinidae) form the largest metazoan family. Combining genomic and cell type transcriptomic insights spanning the largest clade, Aleocharinae, we retrace evolution of two cell types comprising a defensive gland—a putative catalyst behind staphylinid megadiversity. We identify molecular evolutionary steps leading to benzoquinone production by one cell type via a mechanism convergent with plant toxin release systems, and synthesis by the second cell type of a solvent that weaponizes the total secretion. This cooperative system has been conserved since the Early Cretaceous as Aleocharinae radiated into tens of thousands of lineages. Reprogramming each cell type yielded biochemical novelties enabling ecological specialization—most dramatically in symbionts that infiltrate social insect colonies via host-manipulating secretions. Our findings uncover cell type evolutionary processes underlying the origin and evolvability of a beetle chemical innovation.

KW - beetles

KW - biosynthesis

KW - cell type evolution

KW - Dalotia

KW - gene expression programs

KW - genomics

KW - key innovations

KW - Staphylinidae

UR - http://www.scopus.com/inward/record.url?scp=85197553564&partnerID=8YFLogxK

U2 - 10.1016/j.cell.2024.05.012

DO - 10.1016/j.cell.2024.05.012

M3 - Article

C2 - 38889727

AN - SCOPUS:85197553564

SN - 0092-8674

VL - 187

SP - 3563-3584.e26

JO - Cell

JF - Cell

IS - 14

ER -

The genomic and cellular basis of biosynthetic innovation in rove beetles

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