Pangenomic comparison of globally distributed Poribacteria associated with sponge hosts and marine particles

Abstract

Candidatus Poribacteria is a little-known bacterial phylum, previously characterized by partial genomes from a single sponge host, but never isolated in culture. We have reconstructed multiple genome sequences from four different sponge genera and compared them to recently reported, uncharacterized Poribacteria genomes from the open ocean, discovering shared and unique functional characteristics. Two distinct, habitat-linked taxonomic lineages were identified, designated Entoporibacteria (sponge-associated) and Pelagiporibacteria (free-living). These lineages differed in flagellar motility and chemotaxis genes unique to Pelagiporibacteria, and highly expanded families of restriction endonucleases, DNA methylases, transposases, CRISPR repeats, and toxin-antitoxin gene pairs in Entoporibacteria. Both lineages shared pathways for facultative anaerobic metabolism, denitrification, fermentation, organosulfur compound utilization, type IV pili, cellulosomes, and bacterial proteosomes. Unexpectedly, many features characteristic of eukaryotic host association were also shared, including genes encoding the synthesis of eukaryotic-like cell adhesion molecules, extracellular matrix digestive enzymes, phosphoinositol-linked membrane glycolipids, and exopolysaccharide capsules. Complete Poribacteria 16S rRNA gene sequences were found to contain multiple mismatches to "universal" 16S rRNA gene primer sets, substantiating concerns about potential amplification failures in previous studies. A newly designed primer set corrects these mismatches, enabling more accurate assessment of Poribacteria abundance in diverse marine habitats where it may have previously been overlooked.

Genome Sequencing and Analysis of Thraustochytriidae sp. SZU445 Provides Novel Insights into the Polyunsaturated Fatty Acid Biosynthesis Pathway

“…SZU445 by genome sequencing and protein annotation. The KS, KR, and ER were highly homologous to the beta-ketoacyl-acyl-carrier-protein synthase II of Aphanomyces invadans (NCBI accession: XP_008875515.1), oxidoreductase of "Candidatus Poribacteria" bacterium (NCBI accession: RKU36622.1) [35] and tRNA-dihydrouridine(47) synthase NADP+-like of Hondaea fermentalgiana (NCBI accession: GBG27734.1) [30] with approximately 94.45%, 95.67%, and 99.00% identity at the amino acid level. These results demonstrate that Thraustochytrium sp.…”

Chemical Ecology of Marine Sponges: New Opportunities through “-Omics”

“…As a group, their success in these systems is linked to their ability to efficiently remove small particulate matter (phytoplankton, detritus, bacteria, and viruses) from the water via heterotrophic filter feeding (Maldonado et al 2012;McMurray et al 2016). Sponges also host a tremendous diversity of microbial symbionts, with at least 39 microbial (Bacterial and Archaeal) phyla detected in recent large-scale microbiome surveys, with a dominance of the bacterial groups c-, a-, and b-proteobacteria, Actinobacteria, Cyanobacteria, Chloroflexi, and Bacteroidetes, as well as the presence of spongespecific lineages like Poribacteria (Moya et al 2008;Thomas et al 2016;Pita et al 2018;Podell et al 2019). Their success in oligotrophic systems may therefore be linked to an expanded metabolic capacity from these symbiotic associations (Taylor et al 2007;Thacker and Freeman 2012;Freeman et al 2013;McMurray et al 2018).…”

Ecological and biotechnological aspects of Aplysina-associated microorganisms

“…Recently, the discovery of putative Poribacteria-related genomes in samples derived from the open ocean sparked Podell et al (2019) to develop novel universal primers that correct for the mismatches in poribacterial 16S rRNA genes. They report an approximately fivefold higher relative abundance of Poribacteria in various sponge species as compared to EMP primer results (Podell et al, 2019). Thus, these primers should be considered in future diversity analyses since they might be better suitable for reflecting the composition of sponge microbiomes.…”

“…The knowledge on symbiont functions remains limited to date which is partly due to the fact that all of the highly abundant sponge symbionts remain recalcitrant to cultivation. Recent advances in multi-omics techniques however have revealed genetic features of sponge-associated microorganisms that facilitate their symbiotic lifestyle and contribute to the sponge metabolism Astudillo-García et al, 2018;Bayer et al, 2018;Karimi et al, 2018;Kiran et al, 2018;Podell et al, 2019). Some of these processes are illustrated in Figure 5, 1-5, and a few selected symbiotic taxa and their functions are discussed below.…”

“…Poribacterial 16S rRNA genes show more than 25% sequence divergence compared to any other bacterial phylum (Lafi et al, 2009), and contain several mismatches to the widely used Earth Microbiome Project (EMP) primer set (Walters et al, 2015). Thus, microbial profiling studies using the EMP primers might underestimate the abundance of Poribacteria in sponges (Bayer, Kamke, et al, 2014;Podell et al, 2019). Nonetheless, even though relative abundance measures might not be accurate, the EMP primers can successfully amplify poribacterial sequences in DNA of most highmicrobial abundance sponges (Thomas et al 2016 and Figure 2).…”