Comparative Genomics Provides Insight into the Function of Broad-Host Range Sponge Symbionts.

Samantha C Waterworth,Rosemary A Dorrington,Jason C Kwan,Shirley Parker-Nance

doi:10.1128/mbio.01577-21

Samantha C Waterworth, Rosemary A Dorrington + Show 2 more

Open Access

https://doi.org/10.1128/mbio.01577-21

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Journal: mBio	Publication Date: Sep 14, 2021
Citations: 5	License type: CC BY 4.0

Affiliation: Rhodes University, University of Wisconsin–Madison

Abstract

ABSTRACTThe fossil record indicates that the earliest evidence of extant marine sponges (phylum Porifera) existed during the Cambrian explosion and that their symbiosis with microbes may have begun in their extinct ancestors during the Precambrian period. Many symbionts have adapted to their sponge host, where they perform specific, specialized functions. There are also widely distributed bacterial taxa such as Poribacteria, SAUL, and Tethybacterales that are found in a broad range of invertebrate hosts. Here, we added 11 new genomes to the Tethybacterales order, identified a novel family, and show that functional potential differs between the three Tethybacterales families. We compare the Tethybacterales with the well-characterized Entoporibacteria and show that these symbionts appear to preferentially associate with low-microbial abundance (LMA) and high-microbial abundance (HMA) sponges, respectively. Within these sponges, we show that these symbionts likely perform distinct functions and may have undergone multiple association events, rather than a single association event followed by coevolution.

Highlights

The fossil record indicates that the earliest evidence of extant marine sponges existed during the Cambrian explosion and that their symbiosis with microbes may have begun in their extinct ancestors during the Precambrian period
The microbiomes of sponges of the Latrunculiidae family are highly conserved and are dominated by populations of related betaproteobacterial symbionts. These bacteria have since been reclassified as class Gammaproteobacteria, as several betaproteobacteria were, when genome phylogeny was proposed as the basis for taxonomy, which has since been incorporated in the Genome Taxonomy Database (GTDB) [61]
We considered the sponge hosts themselves and found that Entoporibacteria included in this study associate exclusively with high-microbial abundance (HMA) sponges, while the Tethybacterales largely associate with low-microbial abundance (LMA) sponges (Table 3)

Summary

Introduction

The fossil record indicates that the earliest evidence of extant marine sponges (phylum Porifera) existed during the Cambrian explosion and that their symbiosis with microbes may have begun in their extinct ancestors during the Precambrian period. We show that the functional potential of broad-host range symbionts is conserved at a family level and that these symbionts have been acquired several times over evolutionary history It appears that the Entoporibacteria are associated primarily with high-microbial abundance sponges, while the Tethybacterales associate with low-microbial abundance sponges. While their exact time of origin is a subject of hot debate, fossil records indicate that extant marine sponges (phylum Porifera) existed during the Cambrian explosion, approximately 540 million years ago [1, 2], and that symbiotic relationships with microbes may have begun even before the evolution of extant sponge taxa [3]. There was a higher expression of genes involved in 1,2-propanediol degradation and import of vitamin B12, which together suggest that the bacterium may import vitamin B12 as a necessary cofactor for anaerobic 1,2-propanediol degradation and energy generation [42]

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