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Genomic insights from Monoglobus pectinilyticus: a pectin-degrading specialist bacterium in the human colon

The ISME Journal (2019) | Download Citation

Abstract

Pectin is abundant in modern day diets, as it comprises the middle lamellae and one-third of the dry carbohydrate weight of fruit and vegetable cell walls. Currently there is no specialized model organism for studying pectin fermentation in the human colon, as our collective understanding is informed by versatile glycan-degrading bacteria rather than by specialist pectin degraders. Here we show that the genome of Monoglobus pectinilyticus possesses a highly specialized glycobiome for pectin degradation, unique amongst Firmicutes known to be in the human gut. Its genome encodes a simple set of metabolic pathways relevant to pectin sugar utilization, and its predicted glycobiome comprises an unusual distribution of carbohydrate-active enzymes (CAZymes) with numerous extracellular methyl/acetyl esterases and pectate lyases. We predict the M. pectinilyticus degradative process is facilitated by cell-surface S-layer homology (SLH) domain-containing proteins, which proteomics analysis shows are differentially expressed in response to pectin. Some of these abundant cell surface proteins of M. pectinilyticus share unique modular organizations rarely observed in human gut bacteria, featuring pectin-specific CAZyme domains and the cell wall-anchoring SLH motifs. We observed M. pectinilyticus degrades various pectins, RG-I, and galactan to produce polysaccharide degradation products (PDPs) which are presumably shared with other inhabitants of the human gut microbiome (HGM). This strain occupies a new ecological niche for a primary degrader specialized in foraging a habitually consumed plant glycan, thereby enriching our understanding of the diverse community profile of the HGM.

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Acknowledgements

We thank staff at Macrogen (South Korea) and Massey Genome Service (Palmerston North, New Zealand) for sequencing services; and Martin Middleditch and Leo Payne (University of Auckland, New Zealand) for iTRAQ proteomics analysis. We are grateful to Louise Brough (Massey Institute of Food Science and Technology, School of Food and Nutrition, Massey University, Palmerston North, New Zealand), Chrissie Butts (Department of Food, Nutrition and Health, Plant and Food Research Limited, Palmerston North, New Zealand), Rinki Murphy (Faculty of Medical and Health Sciences, The University of Auckland, Auckland, New Zealand), and Jane Coad (Massey Institute of Food Science and Technology, School of Food and Nutrition, Massey University, Palmerston North, New Zealand) for assistance and supervision of the clinical study conducted by GRH during her PhD studies. We thank Peter Janssen at AgResearch Ltd (Grasslands Research Centre, Palmerston North) for providing rumen fluid. We are grateful to David Brummell (Plant and Food Research Limited, Palmerston North) for his valuable advice on pectin structure. This work has been carried out with the financial support of Ministry of Business, Innovation and Employment of New Zealand (‘Foods for Health at Different Life Stages’ C11X1312).

Author contributions

CCK performed all experiments and data analysis related to genome sequencing of M. pectinilyticus. CCK conducted 16S rRNA phylogenetic analysis and quantitative PCR detection of M. pectinilyticus in human faecal samples. GRH designed the clinical study, obtained ethics approval, recruited donors, conducted the study, collected dietary records, and faecal samples, and prepared DNA samples. GH performed the dietary intake analysis. CCK prepared fermented pectin samples, and IMS and TJB assisted with SEC and data analysis. CCK prepared samples for iTRAQ protein quantification, and analysed the data. CCK performed all enzyme phylogeny and metagenome analysis. DH assisted with all statistical analysis used in this study. CAZyme domains were identified by BH using the CAZy database. This study was conceived and supervised by IMS, GWT, WJK, DIR, ZJ, and MLP, and directed by CKK and DIR. All authors contributed to research designing and planning. CCK and DIR wrote the article, with contributions from all other authors.

Author information

Affiliations

  1. The New Zealand Institute for Plant and Food Research, Palmerston North, 4474, New Zealand

    • Caroline C. Kim
    • , Genelle R. Healey
    • , Duncan Hedderley
    •  & Douglas I. Rosendale
  2. Institute of Fundamental Sciences, Massey University, Palmerston North, 4442, New Zealand

    • Caroline C. Kim
    • , Mark L. Patchett
    •  & Zoe Jordens
  3. Massey Institute of Food Science and Technology, School of Food and Nutrition, Massey University, Palmerston North, New Zealand

    • Genelle R. Healey
  4. Donvis Limited, Ashhurst, 4810, New Zealand

    • William J. Kelly
  5. Department of Microbiology and Immunology, Microbiome Otago, University of Otago, Dunedin, 9016, New Zealand

    • Gerald W. Tannock
  6. Ferrier Research Institute, Victoria University of Wellington, Gracefield Research Centre, Lower Hutt, 5040, New Zealand

    • Ian M. Sims
    •  & Tracey J. Bell
  7. Architecture et Fonction des Macromolécules Biologiques, CNRS, Aix-Marseille University, Marseille, F-13288, France

    • Bernard Henrissat
  8. Institut National de la Recherche Agronomique, USC1408 Architecture et Fonction des Macromolécules Biologiques, Marseille, F-13288, France

    • Bernard Henrissat
  9. Department of Biological Sciences, King Abdulaziz University, Jeddah, 21589, Saudi Arabia

    • Bernard Henrissat

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Conflict of interest

The authors declare that they have no conflict of interest.

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Correspondence to Caroline C. Kim or Douglas I. Rosendale.

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DOI

https://doi.org/10.1038/s41396-019-0363-6