Major changes in microbial diversity and community composition across gut sections of a juvenile Panchlora cockroach.

Erin A Gontang,Alison Fern,Frank O Aylward,Cameron R Currie,Camila Carlos,Tijana Glavina Del Rio,Roberto Kolter,Stephanie A Malfatti,Susannah G Tringe,Chien-Chi Lo,Mansi Chovatia

doi:10.1371/journal.pone.0177189

Abstract

Investigations of gut microbiomes have shed light on the diversity and genetic content of these communities, and helped shape our understanding of how host-associated microorganisms influence host physiology, behavior, and health. Despite the importance of gut microbes to metazoans, our understanding of the changes in diversity and composition across the alimentary tract, and the source of the resident community are limited. Here, using community metagenomics and 16S rRNA gene sequencing, we assess microbial community diversity and coding potential in the foregut, midgut, and hindgut of a juvenile Panchlora cockroach, which resides in the refuse piles of the leaf-cutter ant species Atta colombica. We found a significant shift in the microbial community structure and coding potential throughout the three gut sections of Panchlora sp., and through comparison with previously generated metagenomes of the cockroach’s food source and niche, we reveal that this shift in microbial community composition is influenced by the ecosystems in which Panchlora sp. occurs. While the foregut is composed of microbes that likely originate from the symbiotic fungus gardens of the ants, the midgut and hindgut are composed of a microbial community that is likely cockroach-specific. Analogous to mammalian systems, the midgut and hindgut appear to be dominated by Firmicutes and Bacteroidetes with the capacity for polysaccharide degradation, suggesting they may assist in the degradation of dietary plant material. Our work underscores the prominence of community changes throughout gut microbiomes and highlights ecological factors that underpin the structure and function of the symbiotic microbial communities of metazoans.

Highlights

Over the past decade, there has been an increased appreciation for the fundamental roles that gut-microbiota play in the promotion of their host’s health and fitness
Phylogenetic analyses of 16S amplicons from all gut sections indicated that Gammaproteobacteria, Firmicutes, and Bacteroidetes are the dominant bacteria within the juvenile Panchlora cockroach gut (Fig 2A)
Of the 16S amplicons, 61.6% were classified as Gammaproteobacteria, 19.9% were classified as Firmicutes, and 7.3% were classified as Bacteroidetes (Fig 2A)

Summary

Introduction

There has been an increased appreciation for the fundamental roles that gut-microbiota play in the promotion of their host’s health and fitness. Interest in understanding gut microbiomes, coupled with advances in deep sequencing technology, [4,5,6,7,8,9,10,11,12,13,14,15] has provided invaluable insight into the composition and metabolic activities of animal gut microbial communities. Community metagenomics and small subunit (SSU) rRNA gene surveys have provided detailed information regarding the phylogenetic composition of the microbiota inhabiting metazoan guts. Some insects have been found to have highly diverse gut microbiota; cockroaches and termites in particular have been shown to harbor highly diverse microbial communities that help degrade recalcitrant material in the insect’s diet [10, 11, 14, 18, 22,23,24,25,26,27,28,29]. The composition of metazoan gut microbiota has been suggested to change considerably throughout the alimentary tract of the host, likely due to the distinct physical and chemical features of different gut sections, but few studies have investigated these changes directly

Methods

Results

Conclusion