Bacteria Isolated From the Antarctic Sponge Iophon sp. Reveals Mechanisms of Symbiosis in Sporosarcina, Cellulophaga, and Nesterenkonia.

Mario Moreno-Pino,Génesis Parada-Pozo,Nicole Trefault,Susana Rodríguez-Marconi,Jorge H Valdés,Juan A Ugalde

doi:10.3389/fmicb.2021.660779

Abstract

Antarctic sponges harbor a diverse range of microorganisms that perform unique metabolic functions for nutrient cycles. Understanding how microorganisms establish functional sponge–microbe interactions in the Antarctic marine ecosystem provides clues about the success of these ancient animals in this realm. Here, we use a culture-dependent approach and genome sequencing to investigate the molecular determinants that promote a dual lifestyle in three bacterial genera Sporosarcina, Cellulophaga, and Nesterenkonia. Phylogenomic analyses showed that four sponge-associated isolates represent putative novel bacterial species within the Sporosarcina and Nesterenkonia genera and that the fifth bacterial isolate corresponds to Cellulophaga algicola. We inferred that isolated sponge-associated bacteria inhabit similarly marine sponges and also seawater. Comparative genomics revealed that these sponge-associated bacteria are enriched in symbiotic lifestyle-related genes. Specific adaptations related to the cold Antarctic environment are features of the bacterial strains isolated here. Furthermore, we showed evidence that the vitamin B5 synthesis-related gene, panE from Nesterenkonia E16_7 and E16_10, was laterally transferred within Actinobacteria members. Together, these findings indicate that the genomes of sponge-associated strains differ from other related genomes based on mechanisms that may contribute to the life in association with sponges and the extreme conditions of the Antarctic environment.

Highlights

The sponge holobiont- or marine sponge-microorganism assemblage is considered one of the most basal and complex symbiotic relationships and proposed as one of the principal contributors to microbial diversity and functionality across global ocean ecosystems (Ruby, 2008; Pita et al, 2016; Thomas et al, 2016)
The whole-genome analysis presented here allows us to interrogate the genomic adaptations to the symbiotic lifestyle acquired by five Antarctic sponge-associated bacteria belonging to the genera Cellulophaga, Sporosarcina, and Nesterenkonia
Our genomic analysis of five bacterial strains belonging to Cellulophaga, Sporosarcina, and Nesterenkonia reveals that their genomes contain unique genomic adaptations to life associated with the Antarctic sponges

Summary

Introduction

The sponge holobiont- or marine sponge-microorganism assemblage is considered one of the most basal and complex symbiotic relationships and proposed as one of the principal contributors to microbial diversity and functionality across global ocean ecosystems (Ruby, 2008; Pita et al, 2016; Thomas et al, 2016). The establishment of the functional sponge–microbe interaction depends, in part, on a series of molecular determinants that mediate the symbiotic lifestyle adaptation (Gao et al, 2014; Tian et al, 2014, 2016 Burgsdorf et al, 2015; Zhang et al, 2019) These symbiotic signatures include eukaryotic-like protein domains (ELPs), clustered regularly interspaced short palindromic repeats (CRISPR), restriction-modification (RM), and toxin–antitoxin (T-A) systems, which are involved in avoiding the digestion by the sponge host and defending against incoming foreign DNA (Magnuson, 2007; Nguyen et al, 2014; Horn et al, 2016; Díez-Vives et al, 2017; Slaby et al, 2017; Jahn et al, 2019). In the case of the sponge symbiont Candidatus Poribacteria, evidence of symbiotic lifestyle adaptation was inferred based on the loss of the flagellar structure, the presence of exclusive adhesion-related proteins, and a broad set of carbohydrate-degrading enzymes (Siegl et al, 2011; Zhang et al, 2019)

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