Gene sets for utilization of primary and secondary nutrition supplies in the distal gut of endangered Iberian lynx

María Alcaide, Enzo Messina, Michael Richter, Rafael Bargiela, Jörg Peplies, Sharon A Huws, Charles J Newbold, Peter N Golyshin, Miguel A Simón, Guillermo López, Michail M Yakimov, Manuel Ferrer

Research output: Contribution to journalArticleResearchpeer-review

15 Citations (Scopus)

Abstract

Recent studies have indicated the existence of an extensive trans-genomic trans-mural co-metabolism between gut microbes and animal hosts that is diet-, host phylogeny- and provenance-influenced. Here, we analyzed the biodiversity at the level of small subunit rRNA gene sequence and the metabolic composition of 18 Mbp of consensus metagenome sequences and activity characteristics of bacterial intra-cellular extracts, in wild Iberian lynx (Lynx pardinus) fecal samples. Bacterial signatures (14.43% of all of the Firmicutes reads and 6.36% of total reads) related to the uncultured anaerobic commensals Anaeroplasma spp., which are typically found in ovine and bovine rumen, were first identified. The lynx gut was further characterized by an over-representation of 'presumptive' aquaporin aqpZ genes and genes encoding 'active' lysosomal-like digestive enzymes that are possibly needed to acquire glycerol, sugars and amino acids from glycoproteins, glyco(amino)lipids, glyco(amino)glycans and nucleoside diphosphate sugars. Lynx gut was highly enriched (28% of the total glycosidases) in genes encoding α-amylase and related enzymes, although it exhibited low rate of enzymatic activity indicative of starch degradation. The preponderance of β-xylosidase activity in protein extracts further suggests lynx gut microbes being most active for the metabolism of β-xylose containing plant N-glycans, although β-xylosidases sequences constituted only 1.5% of total glycosidases. These collective and unique bacterial, genetic and enzymatic activity signatures suggest that the wild lynx gut microbiota not only harbors gene sets underpinning sugar uptake from primary animal tissues (with the monotypic dietary profile of the wild lynx consisting of 80-100% wild rabbits) but also for the hydrolysis of prey-derived plant biomass. Although, the present investigation corresponds to a single sample and some of the statements should be considered qualitative, the data most likely suggests a tighter, more coordinated and complex evolutionary and nutritional ecology scenario of carnivore gut microbial communities than has been previously assumed.

Original languageEnglish
Pages (from-to)e51521
JournalPLoS ONE
Volume7
Issue number12
DOIs
Publication statusPrint publication - 2012
Externally publishedYes

Fingerprint

Lynx
Nutrition
Xylosidases
Gene encoding
digestive system
Genes
Glycoside Hydrolases
nutrition
Metabolism
Nucleoside Diphosphate Sugars
Polysaccharides
Animals
glycosidases
Sugar Acids
Aquaporins
Anaeroplasma
intestinal microorganisms
genes
Xylose
Biodiversity

Keywords

  • Animals
  • Animals, Wild
  • Bacteria/genetics
  • Endangered Species
  • Feeding Behavior/physiology
  • Gastrointestinal Tract/microbiology
  • Genes, Bacterial/genetics
  • Genetic Variation
  • Lynx/microbiology
  • Spain

Cite this

Alcaide, M., Messina, E., Richter, M., Bargiela, R., Peplies, J., Huws, S. A., ... Ferrer, M. (2012). Gene sets for utilization of primary and secondary nutrition supplies in the distal gut of endangered Iberian lynx. PLoS ONE, 7(12), e51521. https://doi.org/10.1371/journal.pone.0051521
Alcaide, María ; Messina, Enzo ; Richter, Michael ; Bargiela, Rafael ; Peplies, Jörg ; Huws, Sharon A ; Newbold, Charles J ; Golyshin, Peter N ; Simón, Miguel A ; López, Guillermo ; Yakimov, Michail M ; Ferrer, Manuel. / Gene sets for utilization of primary and secondary nutrition supplies in the distal gut of endangered Iberian lynx. In: PLoS ONE. 2012 ; Vol. 7, No. 12. pp. e51521.
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abstract = "Recent studies have indicated the existence of an extensive trans-genomic trans-mural co-metabolism between gut microbes and animal hosts that is diet-, host phylogeny- and provenance-influenced. Here, we analyzed the biodiversity at the level of small subunit rRNA gene sequence and the metabolic composition of 18 Mbp of consensus metagenome sequences and activity characteristics of bacterial intra-cellular extracts, in wild Iberian lynx (Lynx pardinus) fecal samples. Bacterial signatures (14.43{\%} of all of the Firmicutes reads and 6.36{\%} of total reads) related to the uncultured anaerobic commensals Anaeroplasma spp., which are typically found in ovine and bovine rumen, were first identified. The lynx gut was further characterized by an over-representation of 'presumptive' aquaporin aqpZ genes and genes encoding 'active' lysosomal-like digestive enzymes that are possibly needed to acquire glycerol, sugars and amino acids from glycoproteins, glyco(amino)lipids, glyco(amino)glycans and nucleoside diphosphate sugars. Lynx gut was highly enriched (28{\%} of the total glycosidases) in genes encoding α-amylase and related enzymes, although it exhibited low rate of enzymatic activity indicative of starch degradation. The preponderance of β-xylosidase activity in protein extracts further suggests lynx gut microbes being most active for the metabolism of β-xylose containing plant N-glycans, although β-xylosidases sequences constituted only 1.5{\%} of total glycosidases. These collective and unique bacterial, genetic and enzymatic activity signatures suggest that the wild lynx gut microbiota not only harbors gene sets underpinning sugar uptake from primary animal tissues (with the monotypic dietary profile of the wild lynx consisting of 80-100{\%} wild rabbits) but also for the hydrolysis of prey-derived plant biomass. Although, the present investigation corresponds to a single sample and some of the statements should be considered qualitative, the data most likely suggests a tighter, more coordinated and complex evolutionary and nutritional ecology scenario of carnivore gut microbial communities than has been previously assumed.",
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author = "Mar{\'i}a Alcaide and Enzo Messina and Michael Richter and Rafael Bargiela and J{\"o}rg Peplies and Huws, {Sharon A} and Newbold, {Charles J} and Golyshin, {Peter N} and Sim{\'o}n, {Miguel A} and Guillermo L{\'o}pez and Yakimov, {Michail M} and Manuel Ferrer",
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Alcaide, M, Messina, E, Richter, M, Bargiela, R, Peplies, J, Huws, SA, Newbold, CJ, Golyshin, PN, Simón, MA, López, G, Yakimov, MM & Ferrer, M 2012, 'Gene sets for utilization of primary and secondary nutrition supplies in the distal gut of endangered Iberian lynx', PLoS ONE, vol. 7, no. 12, pp. e51521. https://doi.org/10.1371/journal.pone.0051521

Gene sets for utilization of primary and secondary nutrition supplies in the distal gut of endangered Iberian lynx. / Alcaide, María; Messina, Enzo; Richter, Michael; Bargiela, Rafael; Peplies, Jörg; Huws, Sharon A; Newbold, Charles J; Golyshin, Peter N; Simón, Miguel A; López, Guillermo; Yakimov, Michail M; Ferrer, Manuel.

In: PLoS ONE, Vol. 7, No. 12, 2012, p. e51521.

Research output: Contribution to journalArticleResearchpeer-review

TY - JOUR

T1 - Gene sets for utilization of primary and secondary nutrition supplies in the distal gut of endangered Iberian lynx

AU - Alcaide, María

AU - Messina, Enzo

AU - Richter, Michael

AU - Bargiela, Rafael

AU - Peplies, Jörg

AU - Huws, Sharon A

AU - Newbold, Charles J

AU - Golyshin, Peter N

AU - Simón, Miguel A

AU - López, Guillermo

AU - Yakimov, Michail M

AU - Ferrer, Manuel

PY - 2012

Y1 - 2012

N2 - Recent studies have indicated the existence of an extensive trans-genomic trans-mural co-metabolism between gut microbes and animal hosts that is diet-, host phylogeny- and provenance-influenced. Here, we analyzed the biodiversity at the level of small subunit rRNA gene sequence and the metabolic composition of 18 Mbp of consensus metagenome sequences and activity characteristics of bacterial intra-cellular extracts, in wild Iberian lynx (Lynx pardinus) fecal samples. Bacterial signatures (14.43% of all of the Firmicutes reads and 6.36% of total reads) related to the uncultured anaerobic commensals Anaeroplasma spp., which are typically found in ovine and bovine rumen, were first identified. The lynx gut was further characterized by an over-representation of 'presumptive' aquaporin aqpZ genes and genes encoding 'active' lysosomal-like digestive enzymes that are possibly needed to acquire glycerol, sugars and amino acids from glycoproteins, glyco(amino)lipids, glyco(amino)glycans and nucleoside diphosphate sugars. Lynx gut was highly enriched (28% of the total glycosidases) in genes encoding α-amylase and related enzymes, although it exhibited low rate of enzymatic activity indicative of starch degradation. The preponderance of β-xylosidase activity in protein extracts further suggests lynx gut microbes being most active for the metabolism of β-xylose containing plant N-glycans, although β-xylosidases sequences constituted only 1.5% of total glycosidases. These collective and unique bacterial, genetic and enzymatic activity signatures suggest that the wild lynx gut microbiota not only harbors gene sets underpinning sugar uptake from primary animal tissues (with the monotypic dietary profile of the wild lynx consisting of 80-100% wild rabbits) but also for the hydrolysis of prey-derived plant biomass. Although, the present investigation corresponds to a single sample and some of the statements should be considered qualitative, the data most likely suggests a tighter, more coordinated and complex evolutionary and nutritional ecology scenario of carnivore gut microbial communities than has been previously assumed.

AB - Recent studies have indicated the existence of an extensive trans-genomic trans-mural co-metabolism between gut microbes and animal hosts that is diet-, host phylogeny- and provenance-influenced. Here, we analyzed the biodiversity at the level of small subunit rRNA gene sequence and the metabolic composition of 18 Mbp of consensus metagenome sequences and activity characteristics of bacterial intra-cellular extracts, in wild Iberian lynx (Lynx pardinus) fecal samples. Bacterial signatures (14.43% of all of the Firmicutes reads and 6.36% of total reads) related to the uncultured anaerobic commensals Anaeroplasma spp., which are typically found in ovine and bovine rumen, were first identified. The lynx gut was further characterized by an over-representation of 'presumptive' aquaporin aqpZ genes and genes encoding 'active' lysosomal-like digestive enzymes that are possibly needed to acquire glycerol, sugars and amino acids from glycoproteins, glyco(amino)lipids, glyco(amino)glycans and nucleoside diphosphate sugars. Lynx gut was highly enriched (28% of the total glycosidases) in genes encoding α-amylase and related enzymes, although it exhibited low rate of enzymatic activity indicative of starch degradation. The preponderance of β-xylosidase activity in protein extracts further suggests lynx gut microbes being most active for the metabolism of β-xylose containing plant N-glycans, although β-xylosidases sequences constituted only 1.5% of total glycosidases. These collective and unique bacterial, genetic and enzymatic activity signatures suggest that the wild lynx gut microbiota not only harbors gene sets underpinning sugar uptake from primary animal tissues (with the monotypic dietary profile of the wild lynx consisting of 80-100% wild rabbits) but also for the hydrolysis of prey-derived plant biomass. Although, the present investigation corresponds to a single sample and some of the statements should be considered qualitative, the data most likely suggests a tighter, more coordinated and complex evolutionary and nutritional ecology scenario of carnivore gut microbial communities than has been previously assumed.

KW - Animals

KW - Animals, Wild

KW - Bacteria/genetics

KW - Endangered Species

KW - Feeding Behavior/physiology

KW - Gastrointestinal Tract/microbiology

KW - Genes, Bacterial/genetics

KW - Genetic Variation

KW - Lynx/microbiology

KW - Spain

U2 - 10.1371/journal.pone.0051521

DO - 10.1371/journal.pone.0051521

M3 - Article

VL - 7

SP - e51521

JO - PLoS ONE

JF - PLoS ONE

SN - 1932-6203

IS - 12

ER -