Abstract

Relatively little is known about the role of sponge microbiomes in the Antarctic marine environment, where sponges may dominate the benthic landscape. Specifically, we understand little about how taxonomic and functional diversity contributes to the symbiotic lifestyle and aids in nutrient cycling. Here we use functional metagenomics to investigate the community composition and metabolic potential of microbiomes from two abundant Antarctic sponges, Leucetta antarctica and Myxilla sp. Genomic and taxonomic analyses show that both sponges harbor a distinct microbial community with high fungal abundance, which differs from the surrounding seawater. Functional analyses reveal both sponge-associated microbial communities are enriched in functions related to the symbiotic lifestyle (e.g., CRISPR system, Eukaryotic-like proteins, and transposases), and in functions important for nutrient cycling. Both sponge microbiomes possessed genes necessary to perform processes important to nitrogen cycling (i.e., ammonia oxidation, nitrite oxidation, and denitrification), and carbon fixation. The latter indicates that Antarctic sponge microorganisms prefer light-independent pathways for CO2 fixation mediated by chemoautotrophic microorganisms. Together, these results show how the unique metabolic potential of two Antarctic sponge microbiomes help these sponge holobionts survive in these inhospitable environments, and contribute to major nutrient cycles of these ecosystems.

Highlights

  • Little is known about the role of sponge microbiomes in the Antarctic marine environment, where sponges may dominate the benthic landscape

  • We aim to describe the genomic composition of these microbial assemblages and understand how this composition relates to the establishment of symbiosis, nutrient exchange, and sponge holobiont survival

  • This difference in complexity between the sponge and SW microbiomes was further evidenced by GC content differences of individual reads in the metagenomic datasets of sponge-associated and SW communities (Fig. 1b, Table 1)

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Summary

Introduction

Little is known about the role of sponge microbiomes in the Antarctic marine environment, where sponges may dominate the benthic landscape. Genomic and taxonomic analyses show that both sponges harbor a distinct microbial community with high fungal abundance, which differs from the surrounding seawater Functional analyses reveal both sponge-associated microbial communities are enriched in functions related to the symbiotic lifestyle (e.g., CRISPR system, Eukaryotic-like proteins, and transposases), and in functions important for nutrient cycling. Specific molecular determinants of the host-symbiont interaction may include Eukaryotic-like protein domains (ELPs) in the form of proteins with repeated domains (e.g., ankyrin (ARP), tetratricopeptide (TPR), leucine-rich repeats (LRR)), mobile genetic elements (MGEs), and genes related to protection and the stress response (e.g., stress proteins, restriction modification (R-M), toxin-antitoxin (T-A) systems, and clustered regularly interspaced short palindromic repeats (CRISPRs))[9,13] Together, these molecular determinants provide a suite of molecular and physiological adaptations that link the microorganisms to their sponge hosts. Understanding the nature of sponge holobionts in the extreme environment of Antarctica is important since they occupy up to 80% of the benthos and are considered key ecosystem-engineers[25,26]

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