Phages can exploit their bacterial hosts by lytic infection, when many viral particles are released at cell lysis, or by lysogeny, when phages integrate into the host’s genome. We recently proposed a new dynamic model of bacteria–phage interactions in which lysogeny predominates at high microbial abundance and growth rates. This model, named Piggyback-the-Winner (PtW), contrasts to current accepted models on the frequency of lysis and lysogeny and predicts that phages integrate into their hosts’ genomes as prophages when microbial abundances and growth rates are high. According to PtW, switching to the temperate life cycle reduces phage predation control on bacterial abundance and confers superinfection exclusion, preventing that a closely-related phage infects the same bacterial cell. Here we examine how PtW is important for metazoans. Specifically, we postulate that PtW and the recently described bacteriophage adherence to mucus (BAM) model are strongly interrelated and have an important role in the development of the microbiome. In BAM, phage produced by the microbiome attach to mucins and protect underlying epithelial cells from invading bacteria. Spatial structuring of the mucus creates a gradient of phage replication strategies consistent with PtW. We predict that lysogeny is favored at the top mucosal layer and lytic predation predominates in the bacteria-sparse intermediary layers. The lysogeny confers competitive advantage to commensals against niche invasion and the lytic infection eliminates potential pathogens from deeper mucus layers.

Summary: Lysogens are common at high bacterial densities, an observation that contrasts with the prevailing view of lysogeny as a low‐density refugium strategy. Here, we review the mechanisms regulating lysogeny in complex communities and show that the additive effects of coinfections, diversity and host energic status yield a bimodal distribution of lysogeny as a function of microbial densities. At high cell densities (above 10 ⁶ cells ml ⁻¹ or g ⁻¹ ) and low diversity, coinfections by two or more phages are frequent and excess energy availability stimulates inefficient metabolism. Both mechanisms favour phage integration and characterize the Piggyback‐the‐Winner dynamic. At low densities (below 10 ⁵ cells ml ⁻¹ or g ⁻¹ ), starvation represses lytic genes and extends the time window for lysogenic commitment, resulting in a higher frequency of coinfections that cause integration. This pattern follows the predictions of the refugium hypothesis. At intermediary densities (between 10 ⁵ and 10 ⁶ cells ml ⁻¹ or g ⁻¹ ), encounter rates and efficient energy metabolism favour lysis. This may involve Kill‐the‐Winner lytic dynamics and induction. Based on these three regimes, we propose a framework wherein phage integration occurs more frequently at both ends of the host density gradient, with distinct underlying molecular mechanisms (coinfections and host metabolism) dominating at each extreme.

Archaea are ubiquitous symbionts of marine sponges but their ecological roles and the influence of environmental factors on these associations are still poorly understood. We compared the diversity and composition of archaea associated with seawater and with the sponges Hymeniacidon heliophila, Paraleucilla magna and Petromica citrina in two distinct environments: Guanabara Bay, a highly impacted estuary in Rio de Janeiro, Brazil, and the nearby Cagarras Archipelago. For this we used metagenomic analyses of 16S rRNA and ammonia monooxygenase (amoA) gene libraries. Hymeniacidon heliophila was more abundant inside the bay, while P. magna was more abundant outside and P. citrina was only recorded at the Cagarras Archipelago. Principal Component Analysis plots (PCA) generated using pairwise unweighted UniFrac distances showed that the archaeal community structure of inner bay seawater and sponges was different from that of coastal Cagarras Archipelago. Rarefaction analyses showed that inner bay archaeaoplankton were more diverse than those from the Cagarras Archipelago. Only members of Crenarchaeota were found in sponge libraries, while in seawater both Crenarchaeota and Euryarchaeota were observed. Although most amoA archaeal genes detected in this study seem to be novel, some clones were affiliated to known ammonia oxidizers such as Nitrosopumilus maritimus and Cenarchaeum symbiosum. The composition and diversity of archaeal communities associated with pollution-tolerant sponge species can change in a range of few kilometers, probably influenced by eutrophication. The presence of archaeal amoA genes in Porifera suggests that Archaea are involved in the nitrogen cycle within the sponge holobiont, possibly increasing its resistance to anthropogenic impacts. The higher diversity of Crenarchaeota in the polluted area suggests that some marine sponges are able to change the composition of their associated archaeal communities, thereby improving their fitness in impacted environments.

Viruses, microbes, and host macroorganisms form ecological units called holobionts. Here, a combination of metagenomic sequencing, metabolomic profiling, and epifluorescence microscopy was used to investigate how the different components of the holobiont including bacteria, viruses, and their associated metabolites mediate ecological interactions between corals and turf algae. The data demonstrate that there was a microbial assemblage unique to the coral-turf algae interface displaying higher microbial abundances and larger microbial cells. This was consistent with previous studies showing that turf algae exudates feed interface and coral-associated microbial communities, often at the detriment of the coral. Further supporting this hypothesis, when the metabolites were assigned a nominal oxidation state of carbon (NOSC), we found that the turf algal metabolites were significantly more reduced (i.e., have higher potential energy) compared to the corals and interfaces. The algae feeding hypothesis was further supported when the ecological outcomes of interactions (e.g., whether coral was winning or losing) were considered. For example, coral holobionts losing the competition with turf algae had higher Bacteroidetes-to-Firmicutes ratios and an elevated abundance of genes involved in bacterial growth and division. These changes were similar to trends observed in the obese human gut microbiome, where overfeeding of the microbiome creates a dysbiosis detrimental to the long-term health of the metazoan host. Together these results show that there are specific biogeochemical changes at coral–turf algal interfaces that predict the competitive outcomes between holobionts and are consistent with algal exudates feeding coral-associated microbes.