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:

Chase, William R. ^[1]; Zhaxybayeva, Olga ^[2]; Rocha, Jorge  ^[3];

• Search DOE PAGES for author "Rocha, Jorge"
• Search DOE PAGES for ORCID "0000-0002-8083-4325"
• Search orcid.org for ORCID "0000-0002-8083-4325"

Cosgrove, Daniel J. ^[1]; Shapiro, Lori R.  ^[3]

• Search DOE PAGES for author "Shapiro, Lori R."
• Search DOE PAGES for ORCID "0000-0002-8794-6485"
• Search orcid.org for ORCID "0000-0002-8794-6485"

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+ Show Author Affiliations

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:

2020-01-13

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 Name: New Phytologist]; 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