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Title: Global cellulose biomass, horizontal gene transfers and domain fusions drive microbial expansin evolution

Abstract

*Plants must rearrange the network of complex carbohydrates in their cell walls during normal growth and development. To accomplish this, all plants depend on proteins called expansins that non-enzymatically loosen noncovalent bonding between cellulose microfibrils. *Surprisingly, expansin genes have more recently been found in some bacteria and microbial eukaryotes, where their biological functions are largely unknown. *In this work, we reconstruct a comprehensive phylogeny of microbial expansin genes. We find these genes in all eukaryotic microorganisms that have structural cell wall cellulose, suggesting expansins evolved in ancient marine microorganisms long before the evolution of land plants. We also find expansins in an unexpectedly high diversity of bacteria and fungi that do not have cellulosic cell walls. These bacteria and fungi inhabit varied ecological contexts mirroring the diversity of terrestrial and aquatic niches where plant and/or algal cellulosic cell walls are present. *The microbial expansin phylogeny shows evidence of multiple horizontal gene transfer events within and between bacterial and eukaryotic microbial lineages, which may in part underlie their unusually broad phylogenetic distribution. Wholly, expansins are unexpectedly widespread in bacteria and eukaryotes, and the contribution of these genes to microbial ecological interactions with plants and algae has likely been underappreciated.

Authors:
 [1];  [2]; ORCiD logo [3];  [1]; ORCiD logo [3]
  1. Pennsylvania State Univ., University Park, PA (United States)
  2. Dartmouth College, Hanover, NH (United States)
  3. Harvard Medical School, Boston, MA (United States)
Publication Date:
Research Org.:
Pennsylvania State Univ., University Park, PA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES) (SC-22). Chemical Sciences, Geosciences & Biosciences Division; Simons Foundation
OSTI Identifier:
1598351
Grant/Contract Number:  
FG02-84ER13179; ACI‐1548562; DBI‐1202736
Resource Type:
Accepted Manuscript
Journal Name:
New Phytologist
Additional Journal Information:
Journal Volume: 226; Journal ID: ISSN 0028-646X
Publisher:
Wiley
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; expansin; cellulose; horizontal gene transfer; domain fusion; cell wall; plant-microbe interactions; glycoside hydrolase; carbohydrate binding module

Citation Formats

Chase, William R., Zhaxybayeva, Olga, Rocha, Jorge, Cosgrove, Daniel J., and Shapiro, Lori R. Global cellulose biomass, horizontal gene transfers and domain fusions drive microbial expansin evolution. United States: N. p., 2020. Web. doi:10.1111/nph.16428.
Chase, William R., Zhaxybayeva, Olga, Rocha, Jorge, Cosgrove, Daniel J., & Shapiro, Lori R. Global cellulose biomass, horizontal gene transfers and domain fusions drive microbial expansin evolution. United States. doi:https://doi.org/10.1111/nph.16428
Chase, William R., Zhaxybayeva, Olga, Rocha, Jorge, Cosgrove, Daniel J., and Shapiro, Lori R. Mon . "Global cellulose biomass, horizontal gene transfers and domain fusions drive microbial expansin evolution". United States. doi:https://doi.org/10.1111/nph.16428. https://www.osti.gov/servlets/purl/1598351.
@article{osti_1598351,
title = {Global cellulose biomass, horizontal gene transfers and domain fusions drive microbial expansin evolution},
author = {Chase, William R. and Zhaxybayeva, Olga and Rocha, Jorge and Cosgrove, Daniel J. and Shapiro, Lori R.},
abstractNote = {*Plants must rearrange the network of complex carbohydrates in their cell walls during normal growth and development. To accomplish this, all plants depend on proteins called expansins that non-enzymatically loosen noncovalent bonding between cellulose microfibrils. *Surprisingly, expansin genes have more recently been found in some bacteria and microbial eukaryotes, where their biological functions are largely unknown. *In this work, we reconstruct a comprehensive phylogeny of microbial expansin genes. We find these genes in all eukaryotic microorganisms that have structural cell wall cellulose, suggesting expansins evolved in ancient marine microorganisms long before the evolution of land plants. We also find expansins in an unexpectedly high diversity of bacteria and fungi that do not have cellulosic cell walls. These bacteria and fungi inhabit varied ecological contexts mirroring the diversity of terrestrial and aquatic niches where plant and/or algal cellulosic cell walls are present. *The microbial expansin phylogeny shows evidence of multiple horizontal gene transfer events within and between bacterial and eukaryotic microbial lineages, which may in part underlie their unusually broad phylogenetic distribution. Wholly, expansins are unexpectedly widespread in bacteria and eukaryotes, and the contribution of these genes to microbial ecological interactions with plants and algae has likely been underappreciated.},
doi = {10.1111/nph.16428},
journal = {New Phytologist},
number = ,
volume = 226,
place = {United States},
year = {2020},
month = {1}
}

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