Bacterial predation in a marine host-associated microbiome

Abstract

In many ecological communities, predation has a key role in regulating community structure or function. Although predation has been extensively explored in animals and microbial eukaryotes, predation by bacteria is less well understood. Here we show that predatory bacteria of the genus Halobacteriovorax are prevalent and active predators on the surface of several genera of reef-building corals. Across a library of 198 16S rRNA samples spanning three coral genera, 79% were positive for carriage of Halobacteriovorax. Cultured Halobacteriovorax from Porites asteroides corals tested positive for predation on the putative coral pathogens Vibrio corallyticus and Vibrio harveyii. Co-occurrence network analysis showed that Halobacteriovorax's interactions with other bacteria are influenced by temperature and inorganic nutrient concentration, and further suggested that this bacterial predator's abundance may be driven by prey availability. Thus, animal microbiomes can harbor active bacterial predators, which may regulate microbiome structure and protect the host by consuming potential pathogens.

Figure 1

Electron micrographs of our coral-associated strain, Halobacteriovorax PA1, including (a) several attack-phase cells and a Vibrio fortis prey (the single larger cell), (b) a single attack-phase cell, (c) a cell in attachment phase on the surface of a Vibrio fortis prey cell and (d) a Halobacteriovorax entering the prey periplasm. (e) Molecular phylogenetic analysis is based on 16S rRNA gene sequences of the order Bdellovibrionales by the maximum likelihood method. The coral-isolated strain (PA1) used in this study is blue, and strains with whole-genome sequences are red. The bootstrap consensus tree inferred from 500 replicates and bootstrap values >80% are reported. The analysis involved 23 nucleotide sequences. All positions containing gaps and missing data were eliminated. There were a total of 1216 positions in the final data set. Evolutionary analyses were conducted in MEGA6 [3].

Figure 2

Host-associated microbiome networks focused on members of the Bdellovibrionales and like organisms, which include the Halobacteriovorax. Networks were constructed for control samples falling within the temperature bin (a) 23–24 °C and (b) 29–30 °C, and nutrient enrichment samples within the temperature bin (c) 23–24 °C and (d) 29–30 °C. Circles in the networks represent bacterial nodes at order taxa level, color-coded by phylum according to the legend in the center. Blue lines connecting node pairs indicate significant co-occurrence patterns, whereas gray lines denote significant mutual exclusion patterns (P⩽0.05) as determined by the ReBoot randomization procedure in the CoNet Cytoscape package (Faust and Raes, 2012; Faust et al., 2012). Network layout was calculated using edge-weighted spring embedded layout in Cytoscape (Shannon et al., 2003).