High nutrient transport and cycling potential revealed in the microbial metagenome of Australian sea lion (Neophoca cinerea) faeces

Abstract

Metagenomic analysis was used to examine the taxonomic diversity and metabolic potential of an Australian sea lion (Neophoca cinerea) gut microbiome. Bacteria comprised 98% of classifiable sequences and of these matches to Firmicutes (80%) were dominant, with Proteobacteria and Actinobacteria representing 8% and 2% of matches respectively. The relative proportion of Firmicutes (80%) to Bacteriodetes (2%) is similar to that in previous studies of obese humans and obese mice, suggesting the gut microbiome may confer a predisposition towards the excess body fat that is needed for thermoregulation within the cold oceanic habitats foraged by Australian sea lions. Core metabolic functions, including carbohydrate utilisation (14%), protein metabolism (9%) and DNA metabolism (7%) dominated the metagenome, but in comparison to human and fish gut microbiomes there was a significantly higher proportion of genes involved in phosphorus metabolism (2.4%) and iron scavenging mechanisms (1%). When sea lions defecate at sea, the relatively high nutrient metabolism potential of bacteria in their faeces may accelerate the dissolution of nutrients from faecal particles, enhancing their persistence in the euphotic zone where they are available to stimulate marine production.

Figure 1. Taxonomic Diversity of Australian Sea Lion Gut Microbiome.

A: The Australian sea lion gut microbiome was dominated by Firmicutes and Proteobacteria. The following phyla were also present in the ASL gut microbiome but had <10 sequences and thus are not shown on the graph: Aquificae, Viridiplantae, Korarchaeota, Bacteriophage ROSA, Englenozoa, Lactobacillus plantarum bacteriophage phiJL-1, Plasmid PCD4, Plasmid pIP404, Environmental samples, ssRNA negative strand viruses. B: Firmicutes were in turn dominated by Clostridia and Bacilli.

Figure 2. Metabolic Potential of Australian Sea Lion Gut Microbiome.

A: The metabolic potential of the Australian sea lion gut microbiome is dominated by clustering-based subsystems and carbohydrates. Protein metabolism and DNA metabolism are also highly represented. Sequences coding for prophage, secondary metabolism, macromolecular synthesis and dormancy and sporulation were also present but were represented by <10 sequences each and hence are not shown here. B: The metabolic potential of the clustering based subsystems in the Australian sea lion gut microbiome are dominated by clustering based subsystems, cell division and protein export. The following metabolic functions were also present but had <10 sequences and are not shown here: hypothetical associated with RecF, carotenoid biosynthesis, tricarboxylate transporter, probably organic hydroperoxide resistance related hypothetical, protein, pigment biosynthesis, related to N-acetylglucosamine utilization subsystem, TldD cluster, tRNA sulfuration, chemotaxis, response regulators, cluster of unknown function, DNA polymerase III episolon cluster, lipoprotein B cluster, putrescine/GABA utilization cluster, D-tyrosyl-tRNA (Tyr) deacylase (EC′3.1.-.-) cluster, metaylamine utilisation, putative GGDEF doman protein related to agglutinin secretion, and siderophore biosynthesis. C: The clustering-based subsystems were further dominated by clustering-based systems (hierarchical level 3), di- and oligosaccharides, central carbohydrate metabolism, monosaccharides.

Figure 3. Multi-Dimensional Scaling Plot Comparing Australian Sea Lion Microbiome Metabolic Potential with several other Gut, Seawater and Whale Fall Microbiomes.

Metabolic potential of the Australian sea lion gut microbiome is compared to publicly available seawater samples (Antarctic, North Pacific, South Pacific and Indian Oceans), gut microbiomes (human, fish, cow and chicken), and whale fall microbiomes from the MG-RAST server.

Figure 4. Metabolic Subsystems Over-represented and Under-represented in the Australian Sea Lion Faecal Microbiome compared to both Human A and Fish A Gut Microbiomes.

A: The metabolic subsystems that are over-represented in the Australian sea lion faecal microbiome compared to Human A and Fish A gut microbiomes. B: The metabolic subsystems that are under-represented in the Australian sea lion faecal microbiome compared to Human A and Fish A gut microbiomes.

Figure 5. Metabolic Subsystems Over-represented and Under-represented in the Australian Sea Lion Faecal Microbiome compared to two Antarctic Seawater Microbiomes.

A: The metabolic subsystems that are over-represented in the Australian sea lion faecal microbiome compared to two Antarctic seawater microbiomes. B: The metabolic subsystems that are under-represented in the Australian sea lion faecal microbiome compared to two Antarctic seawater microbiomes.