An Insect Herbivore Microbiome with High Plant Biomass-Degrading Capacity

English version České info

Herbivores can gain indirect access to recalcitrant carbon present in plant cell walls through symbiotic associations with lignocellulolytic microbes. A paradigmatic example is the leaf-cutter ant (Tribe: Attini), which uses fresh leaves to cultivate a fungus for food in specialized gardens. Using a combination of sugar composition analyses, metagenomics, and whole-genome sequencing, we reveal that the fungus garden microbiome of leaf-cutter ants is composed of a diverse community of bacteria with high plant biomass-degrading capacity. Comparison of this microbiome's predicted carbohydrate-degrading enzyme profile with other metagenomes shows closest similarity to the bovine rumen, indicating evolutionary convergence of plant biomass degrading potential between two important herbivorous animals. Genomic and physiological characterization of two dominant bacteria in the fungus garden microbiome provides evidence of their capacity to degrade cellulose. Given the recent interest in cellulosic biofuels, understanding how large-scale and rapid plant biomass degradation occurs in a highly evolved insect herbivore is of particular relevance for bioenergy.

Vyšlo v časopise: An Insect Herbivore Microbiome with High Plant Biomass-Degrading Capacity. PLoS Genet 6(9): e32767. doi:10.1371/journal.pgen.1001129
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1001129

Souhrn

Zdroje

1. SticklenMB

2008 Plant genetic engineering for biofuel production: towards affordable cellulosic ethanol. Nat Rev Genet 9 433 443

2. WarneckeF

LuginbuhlP

IvanovaN

GhassemianM

RichardsonTH

2007 Metagenomic and functional analysis of hindgut microbiota of a wood-feeding higher termite. Nature 450 560 565

3. BrulcJM

AntonopoulosDA

MillerME

WilsonMK

YannarellAC

2009 Gene-centric metagenomics of the fiber-adherent bovine rumen microbiome reveals forage specific glycoside hydrolases. Proc Natl Acad Sci U S A 106 1948 1953

4. LeyRE

HamadyM

LozuponeC

TurnbaughPJ

RameyRR

2008 Evolution of mammals and their gut microbes. Science 320 1647 1651

5. TurnbaughPJ

LeyRE

MahowaldMA

MagriniV

MardisER

2006 An obesity-associated gut microbiome with increased capacity for energy harvest. Nature 444 1027 1031

6. GillSR

PopM

DeboyRT

EckburgPB

TurnbaughPJ

2006 Metagenomic analysis of the human distal gut microbiome. Science 312 1355 1359

7. WirthR

HerzH

RyelRJ

BeyschlagW

HolldoblerB

2003 Herbivory of leaf-cutting ants. A case study on Atta colombica in the tropical rain forest of Panama. Springer xvi Berlin, Heidelberg 230

8. WeberNA

1966 Fungus-growing ants. Science 153 587 604

9. CurrieCR

StuartAE

2001 Weeding and grooming of pathogens in agriculture by ants. Proc R Soc London Ser B Biol Sci 268 1033 1039

10. Pinto-TomásAA

AndersenMA

SuenG

StevensonDM

ChuFST

2009 Symbiotic Nitrogen Fixation in the Fungus Gardens of Leaf-cutter Ants. Science 326 1120 1123

11. AbrilAB

BucherEH

2002 Evidence that the fungus cultured by leaf-cutting ants does not metabolize cellulose. Ecology Letters 5 325 328

12. SchiottM

De Fine LichtHH

LangeL

BoomsmaJJ

2008 Towards a molecular understanding of symbiont function: identification of a fungal gene for the degradation of xylan in the fungus gardens of leaf-cutting ants. BMC Microbiol 8 40

13. ErthalMJr

SilvaCP

CooperRM

SamuelsRI

2009 Hydrolytic enzymes of leaf-cutting ant fungi. Comp Biochem Physiol B Biochem Mol Biol 152 54 59

14. MarguliesM

EgholmM

AltmanWE

AttiyaS

BaderJS

2005 Genome sequencing in microfabricated high-density picolitre reactors. Nature 437 376 380

15. LozuponeC

HamadyM

KnightR

2006 UniFrac - An online tool for comparing microbial community diversity in a phylogenetic context. BMC Bioinformatics 7 371

16. HolmesAJ

TujulaNA

HolleyM

ContosA

JamesJM

2001 Phylogenetic structure of unusual aquatic microbial formations in Nullarbor caves, Australia. Environ Microbiol 3 256 264

17. HugenholtzP

PitulleC

HershbergerKL

PaceNR

1998 Novel division level bacterial diversity in a Yellowstone hot spring. J Bacteriol 180 366 376

18. RheimsH

RaineyFA

StackebrandtE

1996 A molecular approach to search for diversity among bacteria in the environment. Journal of Industrial Microbiology and Biotechnology 17 159 169

19. LipsonDA

SchmidtSK

2004 Seasonal changes in an alpine soil bacterial community in the colorado rocky mountains. Appl Environ Microbiol 70 2867 2879

20. HugenholtzP

GoebelBM

PaceNR

1998 Impact of culture-independent studies on the emerging phylogenetic view of bacterial diversity. J Bacteriol 180 4765 4774

21. von MeringC

HugenholtzP

RaesJ

TringeSG

DoerksT

2007 Quantitative phylogenetic assessment of microbial communities in diverse environments. Science 315 1126 1130

22. BradyA

SalzbergSL

2009 Phymm and PhymmBL: metagenomic phylogenetic classification with interpolated Markov models. Nat Methods 6 673 676

23. CantarelBL

CoutinhoPM

RancurelC

BernardT

LombardV

2009 The Carbohydrate-Active EnZymes database (CAZy): an expert resource for Glycogenomics. Nucleic Acids Res 37 D233 238

24. WeimerPJ

RussellJB

MuckRE

2009 Lessons from the cow: what the ruminant animal can teach us about consolidated bioprocessing of cellulosic biomass. Bioresour Technol 100 5323 5331

25. WeimerPJ

StevensonDM

MertensDR

ThomasEE

2008 Effect of monensin feeding and withdrawal on populations of individual bacterial species in the rumen of lactating dairy cows fed high-starch rations. Appl Microbiol Biotechnol 80 135 145

26. PfisterCA

MeyerF

AntonopoulosDA

2010 Metagenomic Profiling of a Microbial Assemblage Associated with the California Mussel: A Node in Networks of Carbon and Nitrogen Cycling. PLoS ONE 5 e10518doi:10.1371/journal.pone.0010518

27. RuschDB

HalpernAL

SuttonG

HeidelbergKB

WilliamsonS

2007 The Sorcerer II Global Ocean Sampling expedition: northwest Atlantic through eastern tropical Pacific. PLoS Biol 5 e77 doi:10.1371/journal.pbio.0050077

28. DillonRJ

DillonVM

2004 The gut bacteria of insects: nonpathogenic interactions. Annu Rev Entomol 49 71 92

29. BroderickNA

RaffaKF

GoodmanRM

HandelsmanJ

2004 Census of the bacterial community of the gypsy moth larval midgut by using culturing and culture-independent methods. Appl Environ Microbiol 70 293 300

30. RussellJA

MoreauCS

Goldman-HuertasB

FujiwaraM

LohmanDJ

2009 Bacterial gut symbionts are tightly linked with the evolution of herbivory in ants. Proc Natl Acad Sci U S A

31. UpdegraffDM

1969 Semimicro determination of cellulose in biological materials. Analytical Biochemistry 32 420 424

32. SelvendraRR

O'NeillMA

1987 Isolation and analysis of cell walls from plant material.

DavidG

Methods of Biochemical Analysis: John Wiley & Sons 25 153

33. YorkWS

DarvillAG

McNeilT

StevensonTT

AlbersheimP

1985 Isolation and characterization of plant cell walls and cell wall components. Methods in Enzymology 118 3 40

34. AlbersheimP

NevinsDJ

EnglishPD

KarrA

1967 A method for the analysis of sugars in plant cell wall polysaccharides by gas-liquid chromatography. Carbohydrate Research 5 340 345

35. JungHJ

VarelVH

WeimerPJ

RalphJ

1999 Accuracy of Klason lignin and acid detergent lignin methods as assessed by bomb calorimetry. J Agric Food Chem 47 2005 2008

36. ApajalahtiJHA

SarkilahtiLK

MakiBRE

HeikkinenJP

NurminenPH

1998 Effective Recovery of Bacterial DNA and Percent-Guanine-Plus-Cytosine-Based Analysis of Community Structure in the Gastrointestinal Tract of Broiler Chickens. Applied and Environmental Microbiology 64 4084

37. AltschulSF

MaddenTL

SchafferAA

ZhangJ

ZhangZ

1997 Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25 3389 3402

38. AshelfordKE

ChuzhanovaNA

FryJC

JonesAJ

WeightmanAJ

2006 New screening software shows that most recent large 16S rRNA gene clone libraries contain chimeras. Appl Environ Microbiol 72 5734 5741

39. HuberT

FaulknerG

HugenholtzP

2004 Bellerophon: a program to detect chimeric sequences in multiple sequence alignments. Bioinformatics 20 2317 2319

40. LudwigW

StrunkO

WestramR

RichterL

MeierH

2004 ARB: a software environment for sequence data. Nucleic Acids Res 32 1363 1371

41. PruesseE

QuastC

KnittelK

FuchsBM

LudwigW

2007 SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucleic Acids Res 35 7188 7196

42. FelensteinJ

1989 PHYLIP - Phylogeny Inference Package (Version 3.2). Cladistics 5

43. SchlossPD

WestcottSL

RyabinT

HallJR

HartmannM

2009 Introducing mothur: Open Source, Platform-independent, Community-supported Software for Describing and Comparing Microbial Communities. Appl Environ Microbiol

44. StamatakisA

LudwigT

MeierH

2005 RAxML-III: a fast program for maximum likelihood-based inference of large phylogenetic trees. Bioinformatics 21 456 463

45. ColeJR

WangQ

CardenasE

FishJ

ChaiB

2009 The Ribosomal Database Project: improved alignments and new tools for rRNA analysis. Nucleic Acids Research 37 D141

46. DeSantisTZ

HugenholtzP

LarsenN

RojasM

BrodieEL

2006 Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl Environ Microbiol 72 5069 5072

47. ShenemanL

EvansJ

FosterJA

2006 Clearcut: a fast implementation of relaxed neighbor joining. Bioinformatics 22 2823

48. BesemerJ

BorodovskyM

2005 GeneMark: web software for gene finding in prokaryotes, eukaryotes and viruses. Nucleic Acids Res 33 W451 454

49. FinnRD

TateJ

MistryJ

CoggillPC

SammutSJ

2008 The Pfam protein families database. Nucleic Acids Res 36 D281 288

50. Marchler-BauerA

AndersonJB

DerbyshireMK

DeWeese-ScottC

GonzalesNR

2007 CDD: a conserved domain database for interactive domain family analysis. Nucleic Acids Res 35 D237 240

51. TringeSG

von MeringC

KobayashiA

SalamovAA

ChenK

2005 Comparative metagenomics of microbial communities. Science 308 554 557

52. TatusovRL

GalperinMY

NataleDA

KooninEV

2000 The COG database: a tool for genome-scale analysis of protein functions and evolution. Nucleic Acids Res 28 33 36

53. QuA

BrulcJM

WilsonMK

LawBF

TheoretJR

2008 Comparative metagenomics reveals host specific metavirulomes and horizontal gene transfer elements in the chicken cecum microbiome. PLoS One 3 e2945 doi:10.1371/journal.pone.0002945

54. DinsdaleEA

EdwardsRA

HallD

AnglyF

BreitbartM

2008 Functional metagenomic profiling of nine biomes. Nature 452 629 632

55. WoykeT

TeelingH

IvanovaNN

HuntemannM

RichterM

2006 Symbiosis insights through metagenomic analysis of a microbial consortium. Nature 443 950 955

56. KurokawaK

ItohT

KuwaharaT

OshimaK

TohH

2007 Comparative metagenomics revealed commonly enriched gene sets in human gut microbiomes. DNA Res 14 169 181

57. Garcia MartinH

IvanovaN

KuninV

WarneckeF

BarryKW

2006 Metagenomic analysis of two enhanced biological phosphorus removal (EBPR) sludge communities. Nat Biotechnol 24 1263 1269

58. GordonD

AbajianC

GreenP

1998 Consed: a graphical tool for sequence finishing. Genome Res 8 195 202

59. EwingB

GreenP

1998 Base-calling of automated sequencer traces using phred. II. Error probabilities. Genome Res 8 186 194

60. EwingB

HillierL

WendlMC

GreenP

1998 Base-calling of automated sequencer traces using phred. I. Accuracy assessment. Genome Res 8 175 185

61. CarverT

ThomsonN

BleasbyA

BerrimanM

ParkhillJ

2009 DNAPlotter: circular and linear interactive genome visualization. Bioinformatics 25 119 120

62. UlrichA

KlimkeG

WirthS

2008 Diversity and activity of cellulose-decomposing bacteria, isolated from a sandy and a loamy soil after long-term manure application. Microb Ecol 55 512 522