Interspecies interactions are an integral determinant of microbial community dynamics.

Fatma A A Aziz,Yasuhisa Saito,Akira Hiraishi,Naoko Mizuno,Hidetaka Hirai,Keita Sagegami,Jun Seno,Akihiro Ohtaki,Hiroyuki Futamata,Kenshi Suzuki,Yuma Inuzuka,Yosuke Tashiro

doi:10.3389/fmicb.2015.01148

Abstract

This study investigated the factors that determine the dynamics of bacterial communities in a complex system using multidisciplinary methods. Since natural and engineered microbial ecosystems are too complex to study, six types of synthetic microbial ecosystems (SMEs) were constructed under chemostat conditions with phenol as the sole carbon and energy source. Two to four phenol-degrading, phylogenetically and physiologically different bacterial strains were used in each SME. Phylogeny was based on the nucleotide sequence of 16S rRNA genes, while physiologic traits were based on kinetic and growth parameters on phenol. Two indices, J parameter and “interspecies interaction,” were compared to predict which strain would become dominant in an SME. The J parameter was calculated from kinetic and growth parameters. On the other hand, “interspecies interaction,” a new index proposed in this study, was evaluated by measuring the specific growth activity, which was determined on the basis of relative growth of a strain with or without the supernatant prepared from other bacterial cultures. Population densities of strains used in SMEs were enumerated by real-time quantitative PCR (qPCR) targeting the gene encoding the large subunit of phenol hydroxylase and were compared to predictions made from J parameter and interspecies interaction calculations. In 4 of 6 SEMs tested the final dominant strain shown by real-time qPCR analyses coincided with the strain predicted by both the J parameter and the interspecies interaction. However, in SMEII-2 and SMEII-3 the final dominant Variovorax strains coincided with prediction of the interspecies interaction but not the J parameter. These results demonstrate that the effects of interspecies interactions within microbial communities contribute to determining the dynamics of the microbial ecosystem.

Highlights

Microbial populations influence each other during the development of their ecosystems, while at the same time the microbial ecosystem is affected by its surrounding environments and vice versa (Fernández et al, 2000; Hashsham et al, 2000; Little et al, 2008; Klitgord and Segrè, 2010)
In a soil bioreactor fed with phenol we previously observed a unique phenomenon where the kinetic parameters shifted toward higher KS and lower KI-values (Futamata et al, 2005; Haruta et al, 2013)
By observing changes in population densities we have developed a better understanding of population dynamics in synthetic microbial ecosystems (SMEs) and soil bioreactors

Summary

Introduction

Microbial populations influence each other during the development of their ecosystems, while at the same time the microbial ecosystem is affected by its surrounding environments and vice versa (Fernández et al, 2000; Hashsham et al, 2000; Little et al, 2008; Klitgord and Segrè, 2010). It is predicted that the sustainability of an ecosystem will be maintained by dynamic changes of the bacterial community (dynamic equilibrium) (Ishii et al, 2012; Yamamoto et al, 2014). We previously observed a unique phenomenon of bacterial population dynamics in a chemostat soil bioreactor enriched with phenol (Futamata et al, 2005). Members of Variovorax exhibiting lower affinities for phenol constituted the final dominant population in this soil bioreactor (Futamata et al, 2005). This result indicated that kinetic parameters are not necessarily the sole determinant for predicting bacterial community dynamics in a chemostat culture. Further research is necessary to unveil the mechanism by which the Variovorax species became dominant in a complex chemostat ecosystem despite exhibiting lower affinity for phenol

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