Fungal endophytes as priority colonizers initiating wood decomposition

Zewei Song, Peter G Kennedy, Feng J. Liew, Jonathan S Schilling

Research output: Contribution to journalArticle

26 Citations (Scopus)

Abstract

Priority effects among wood decomposers have been demonstrated by manipulating fungal assembly history via inoculations in dead wood and then tracking community development using DNA sequencing. Individual wood-degrading fungi have been shown, however, to initiate decay after having colonized living trees as endophytes. To track these ‘upstream’ colonizers across the endophyte–saprophyte transition, we coupled high-throughput sequencing with wood physiochemical analyses in stem sections extracted from healthy birch trees (Betula papyrifera; 4–7 cm dia.). We incubated wood in microcosms, limiting communities as endophytes−only or challenging endophytes with Fomes fomentarius or Piptoporus betulinus at high exogenous inoculum potential. Initial fungal richness in birch stems averaged 143 OTUs and decreased nearly threefold after five months of decomposition. Although F. fomentarius successfully colonized some stem sections incubated at 25 °C, decayed wood was generally dominated by saprophytic fungi that were present originally in lower abundances as endophytes. Among saprophytes, fungi in the brown rot functional guild consistently dominated, matching wood residues bearing the chemical hallmarks of brown rot. Despite this functionally redundant outcome, the taxa that rose to dominate in individual sections varied. Surprisingly, the brown rot taxa dominating wood decomposition were better known for lumber degradation rather than log decay in ground contact. Given the isolation from colonizers in our design, this redundancy of brown rot as the outcome suggests that these taxa and more generally brown rot fungi could have adapted to decompose wood where there is lower competitive pressure. Competitive avoidance would complement the diffuse depolymerization mechanisms of brown rot fungi, which are likely more prone to sugar pilfering by other organisms than the processive depolymerization mechanisms of white rot fungi. Overall, this guild-level predictability of fungal endophyte development and consequence is encouraging given the challenges of predicting wood decomposition, and it provides a base for testing these dynamics under increasing natural complexity.

Original languageEnglish (US)
Pages (from-to)407-418
Number of pages12
JournalFunctional Ecology
Volume31
Issue number2
DOIs
StatePublished - Feb 1 2017

Fingerprint

decayed wood
endophyte
endophytes
brown-rot fungi
decomposition
fungus
depolymerization
Betula
stems
Piptoporus
Fomes fomentarius
deterioration
dynamic testing
Otus
wood residues
saprophytes
Betula papyrifera
white-rot fungi
stem
fungi

Keywords

  • brown rot
  • durability
  • endophytic
  • fungal community
  • historical contingency
  • latent
  • lignocellulose
  • white rot

Cite this

Fungal endophytes as priority colonizers initiating wood decomposition. / Song, Zewei; Kennedy, Peter G; Liew, Feng J.; Schilling, Jonathan S.

In: Functional Ecology, Vol. 31, No. 2, 01.02.2017, p. 407-418.

Research output: Contribution to journalArticle

@article{79145571934f4685bddaa624fa300188,
title = "Fungal endophytes as priority colonizers initiating wood decomposition",
abstract = "Priority effects among wood decomposers have been demonstrated by manipulating fungal assembly history via inoculations in dead wood and then tracking community development using DNA sequencing. Individual wood-degrading fungi have been shown, however, to initiate decay after having colonized living trees as endophytes. To track these ‘upstream’ colonizers across the endophyte–saprophyte transition, we coupled high-throughput sequencing with wood physiochemical analyses in stem sections extracted from healthy birch trees (Betula papyrifera; 4–7 cm dia.). We incubated wood in microcosms, limiting communities as endophytes−only or challenging endophytes with Fomes fomentarius or Piptoporus betulinus at high exogenous inoculum potential. Initial fungal richness in birch stems averaged 143 OTUs and decreased nearly threefold after five months of decomposition. Although F. fomentarius successfully colonized some stem sections incubated at 25 °C, decayed wood was generally dominated by saprophytic fungi that were present originally in lower abundances as endophytes. Among saprophytes, fungi in the brown rot functional guild consistently dominated, matching wood residues bearing the chemical hallmarks of brown rot. Despite this functionally redundant outcome, the taxa that rose to dominate in individual sections varied. Surprisingly, the brown rot taxa dominating wood decomposition were better known for lumber degradation rather than log decay in ground contact. Given the isolation from colonizers in our design, this redundancy of brown rot as the outcome suggests that these taxa and more generally brown rot fungi could have adapted to decompose wood where there is lower competitive pressure. Competitive avoidance would complement the diffuse depolymerization mechanisms of brown rot fungi, which are likely more prone to sugar pilfering by other organisms than the processive depolymerization mechanisms of white rot fungi. Overall, this guild-level predictability of fungal endophyte development and consequence is encouraging given the challenges of predicting wood decomposition, and it provides a base for testing these dynamics under increasing natural complexity.",
keywords = "brown rot, durability, endophytic, fungal community, historical contingency, latent, lignocellulose, white rot",
author = "Zewei Song and Kennedy, {Peter G} and Liew, {Feng J.} and Schilling, {Jonathan S}",
year = "2017",
month = "2",
day = "1",
doi = "10.1111/1365-2435.12735",
language = "English (US)",
volume = "31",
pages = "407--418",
journal = "Functional Ecology",
issn = "0269-8463",
publisher = "Wiley-Blackwell",
number = "2",

}

TY - JOUR

T1 - Fungal endophytes as priority colonizers initiating wood decomposition

AU - Song, Zewei

AU - Kennedy, Peter G

AU - Liew, Feng J.

AU - Schilling, Jonathan S

PY - 2017/2/1

Y1 - 2017/2/1

N2 - Priority effects among wood decomposers have been demonstrated by manipulating fungal assembly history via inoculations in dead wood and then tracking community development using DNA sequencing. Individual wood-degrading fungi have been shown, however, to initiate decay after having colonized living trees as endophytes. To track these ‘upstream’ colonizers across the endophyte–saprophyte transition, we coupled high-throughput sequencing with wood physiochemical analyses in stem sections extracted from healthy birch trees (Betula papyrifera; 4–7 cm dia.). We incubated wood in microcosms, limiting communities as endophytes−only or challenging endophytes with Fomes fomentarius or Piptoporus betulinus at high exogenous inoculum potential. Initial fungal richness in birch stems averaged 143 OTUs and decreased nearly threefold after five months of decomposition. Although F. fomentarius successfully colonized some stem sections incubated at 25 °C, decayed wood was generally dominated by saprophytic fungi that were present originally in lower abundances as endophytes. Among saprophytes, fungi in the brown rot functional guild consistently dominated, matching wood residues bearing the chemical hallmarks of brown rot. Despite this functionally redundant outcome, the taxa that rose to dominate in individual sections varied. Surprisingly, the brown rot taxa dominating wood decomposition were better known for lumber degradation rather than log decay in ground contact. Given the isolation from colonizers in our design, this redundancy of brown rot as the outcome suggests that these taxa and more generally brown rot fungi could have adapted to decompose wood where there is lower competitive pressure. Competitive avoidance would complement the diffuse depolymerization mechanisms of brown rot fungi, which are likely more prone to sugar pilfering by other organisms than the processive depolymerization mechanisms of white rot fungi. Overall, this guild-level predictability of fungal endophyte development and consequence is encouraging given the challenges of predicting wood decomposition, and it provides a base for testing these dynamics under increasing natural complexity.

AB - Priority effects among wood decomposers have been demonstrated by manipulating fungal assembly history via inoculations in dead wood and then tracking community development using DNA sequencing. Individual wood-degrading fungi have been shown, however, to initiate decay after having colonized living trees as endophytes. To track these ‘upstream’ colonizers across the endophyte–saprophyte transition, we coupled high-throughput sequencing with wood physiochemical analyses in stem sections extracted from healthy birch trees (Betula papyrifera; 4–7 cm dia.). We incubated wood in microcosms, limiting communities as endophytes−only or challenging endophytes with Fomes fomentarius or Piptoporus betulinus at high exogenous inoculum potential. Initial fungal richness in birch stems averaged 143 OTUs and decreased nearly threefold after five months of decomposition. Although F. fomentarius successfully colonized some stem sections incubated at 25 °C, decayed wood was generally dominated by saprophytic fungi that were present originally in lower abundances as endophytes. Among saprophytes, fungi in the brown rot functional guild consistently dominated, matching wood residues bearing the chemical hallmarks of brown rot. Despite this functionally redundant outcome, the taxa that rose to dominate in individual sections varied. Surprisingly, the brown rot taxa dominating wood decomposition were better known for lumber degradation rather than log decay in ground contact. Given the isolation from colonizers in our design, this redundancy of brown rot as the outcome suggests that these taxa and more generally brown rot fungi could have adapted to decompose wood where there is lower competitive pressure. Competitive avoidance would complement the diffuse depolymerization mechanisms of brown rot fungi, which are likely more prone to sugar pilfering by other organisms than the processive depolymerization mechanisms of white rot fungi. Overall, this guild-level predictability of fungal endophyte development and consequence is encouraging given the challenges of predicting wood decomposition, and it provides a base for testing these dynamics under increasing natural complexity.

KW - brown rot

KW - durability

KW - endophytic

KW - fungal community

KW - historical contingency

KW - latent

KW - lignocellulose

KW - white rot

UR - http://www.scopus.com/inward/record.url?scp=84989227403&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=84989227403&partnerID=8YFLogxK

U2 - 10.1111/1365-2435.12735

DO - 10.1111/1365-2435.12735

M3 - Article

AN - SCOPUS:84989227403

VL - 31

SP - 407

EP - 418

JO - Functional Ecology

JF - Functional Ecology

SN - 0269-8463

IS - 2

ER -