Network-guided genomic and metagenomic analysis of the faecal microbiota of the critically endangered kakapo

David W Waite,Philip Hugenholtz,Michael W Taylor,Melissa Dsouza,Yuji Sekiguchi

doi:10.1038/s41598-018-26484-4

Abstract

The kakapo is a critically endangered, herbivorous parrot endemic to New Zealand. The kakapo hindgut hosts a dense microbial community of low taxonomic diversity, typically dominated by Escherichia fergusonii, and has proven to be a remarkably stable ecosystem, displaying little variation in core membership over years of study. To elucidate mechanisms underlying this robustness, we performed 16S rRNA gene-based co-occurrence network analysis to identify potential interactions between E. fergusonii and the wider bacterial community. Genomic and metagenomic sequencing were employed to facilitate interpretation of potential interactions observed in the network. E. fergusonii maintained very few correlations with other members of the microbiota, and isolates possessed genes for the generation of energy from a wide range of carbohydrate sources, including plant fibres such as cellulose. We surmise that this dominant microorganism is abundant not due to ecological interaction with other members of the microbiota, but its ability to metabolise a wide range of nutrients in the gut. This research represents the first concerted effort to understand the functional roles of the kakapo microbiota, and leverages metagenomic data to contextualise co-occurrence patterns. By combining these two techniques we provide a means for studying the diversity-stability hypothesis in the context of bacterial ecosystems.

Highlights

The kakapo (Strigops habroptilus) is an endemic New Zealand parrot, known for its unusual diet, nocturnal behaviour and lack of flight
Gastrointestinal (GI) tract-associated bacteria have been of interest for over half a century[5] and have been linked to improved energy harvest from food sources[6,7,8], vitamin and nutrient synthesis[9,10,11], and gut development[12,13]
Adaptation to herbivory the resident microbiota plays a critical role in the depolymerisation of cellulose and hemicellulose into sugars that are accessible to the host[8,18,19]

Summary

Introduction

The kakapo (Strigops habroptilus) is an endemic New Zealand parrot, known for its unusual diet, nocturnal behaviour and lack of flight. Co-occurrence networks of microbial communities represent a means to bridge such limitations, allowing researchers to identify population subsets within a microbiota that may be interacting in either a beneficial or antagonistic manner. In this approach, individual species (or operational taxonomic units – OTUs) are represented by nodes in a web, connected by predicted interactions with other species[27,28,29]. Network analysis provides other metrics to analyse the community through measures such as the degree of community fragmentation[31]

Objectives

Methods

Results