Nematode endosymbiont competition: Fortune favors the fittest

Highlights

• Entomopathogenic nematodes and their bacteria colonize insects as a complex.

• Bacterial preference confers reproductive advantage to certain nematodes.

• Co-evolutionary fitness determines the success of the nematode-bacteria complex.

• Nematode-bacteria competition is a model to study vector-parasite competition.

Abstract

Endosymbiotic bacteria that obligately associate with entomopathogenic nematodes as a complex are a unique model system to study competition. These nematodes seek an insect host and provide entry for their endosymbionts. Through their natural products, the endosymbionts nurture their nematodes by eliminating secondary infection, providing nutrients through bioconversion of the insect cadaver, and facilitating reproduction. On one hand, they cooperatively colonize the insect host and neutralize other opportunistic biotic threats. On the other hand, inside the insect cadaver as a fighting pit, they fiercely compete for the fittest partnership that will grant them the reproductive dominance. Here, we review the protective and nurturing nature of endosymbiotic bacteria for their nematodes and how their selective preference shapes the superior nematode-endosymbiont pairs as we know today.

Introduction

Terrestrial nematodes that are symbiotically associated with bacteria have been used for nearly 60 years as commercial biological control agents for pest management in agricultural crops and combatting the mosquitos Culex pipiens [1] and Aedes sp. [2]. Two nematode genera that stand out for this purpose are Heterorhabditis and Steinernema, harboring Photorhabdus and Xenorhabdus symbiotic bacteria, respectively [3]. Apart from their usage as biological insecticides, the unique interaction of these nematode-endosymbiont complexes offers an invaluable tool as a model system to study the dynamics of competition interweaved with the evolution of mutualism.

The life cycle of Heterorhabditis and Steinernema nematodes involves two different phases: a non-feeding phase, in which the nematode infective juveniles (IJs) are seeking environmental cues to find a host, and a parasitic phase, in which the IJs develop into adults and reproduce inside the insect host (Fig. 1). On the other hand, the life cycle of endosymbionts are divided into three phases: (i) phoretic phase, where the endosymbionts are slowly replicating inside their nematode; (ii) pathogenic phase, after they reach the insect hemolymph and start invading the insect host; and (iii) saprophytic phase, where they bioconvert the insect cadaver for their nematode and re-associate with the new generation of nematode IJs as the food depletes [4].

In general, the interactions between nematodes and their native symbionts are mutualistic. The nematodes provide entry to the insect host [5], while the endosymbionts offer protection and allow nematode replication within the insect host [6]. However, during the non-feeding stage, the nematode IJs must modulate the distribution of their stored energy to sustain themselves while supporting the replication of their endosymbiotic bacteria until they can find a suitable insect host to parasitize and exploit for their own benefit [7].

During the parasitic phase, entomopathogenic nematodes aim to colonize the insect host for reproduction. For them, the degree of fitness, and therefore benefits, brought by the symbiotic bacteria can confer competitive advantage in the success rate of insect host infection and the replication of the parasite [8]. For the symbiont, enabling development and high proliferation for their preferred nematodes mean the “champion” bacteria will be transmitted and re-associate with the new generation of IJs emerging from the insect cadaver. Thereby, the entomopathogenic nematode life cycle is re-started as a non-feeding IJ.

A recent publication challenged the notion of the monoxeny of endosymbiotic bacteria and identified various frequently-associated microbiota (FAM) carried by the nematodes emerging from the insect cadaver [9]. The bacteria identified as FAM were found to be cultivatable Proteobacteria that are pathogenic to insect larvae. This mini review, however, will focus on the endosymbiotic bacteria that have been characterized partners of the entomopathogenic nematodes Heterorhabditis and Steinernema. In particular, the bacteria that enable sexual reproduction of the nematodes on top of their roles in insect host pathogenicity and bioconversion.

We will review the molecular tools used by endosymbiotic bacteria to overcome the harsh biotic threats to emerge from the insect cadaver as a complex with their nematodes. In addition, this review will also explore the competition dynamics among endosymbionts and the biological basis underlying the co-evolution of natural partnership with their cognate nematodes.