Relationship between bacterial phylotype and specialized metabolite production in the culturable microbiome of two freshwater sponges

Abstract

Microbial drug discovery programs rely heavily on accessing bacterial diversity from the environment to acquire new specialized metabolite (SM) lead compounds for the therapeutic pipeline. Therefore, knowledge of how commonly culturable bacterial taxa are distributed in nature, in addition to the degree of variation of SM production within those taxa, is critical to informing these front-end discovery efforts and making the overall sample collection and bacterial library creation process more efficient. In the current study, we employed MALDI-TOF mass spectrometry and the bioinformatics pipeline IDBac to analyze diversity within phylotype groupings and SM profiles of hundreds of bacterial isolates from two Eunapius fragilis freshwater sponges, collected 1.5 km apart. We demonstrated that within two sponge samples of the same species, the culturable bacterial populations contained significant overlap in approximate genus-level phylotypes but mostly nonoverlapping populations of isolates when grouped lower than the level of genus. Further, correlations between bacterial phylotype and SM production varied at the species level and below, suggesting SM distribution within bacterial taxa must be analyzed on a case-by-case basis. Our results suggest that two E. fragilis freshwater sponges collected in similar environments can exhibit large culturable diversity on a species-level scale, thus researchers should scrutinize the isolates with analyses that take both phylogeny and SM production into account to optimize the chemical space entering into a downstream bacterial library.

First report on pollutant accumulation and associated microbial communities in the freshwater sponge Spongilla lacustris (Linnaeus, 1759) from the sub‐Arctic Pasvik River (Norway)

“…To date, there are very few studies on the diversity of the bacterial communities associated with freshwater sponges (Belikov et al, 2019; Clark et al, 2022; Costa et al, 2013; Gaikwad et al, 2016; Gernert et al, 2005; Kaluzhnaya et al, 2011; Kaluzhnaya & Itskovich, 2014, 2016; Kenny et al, 2019; Laport et al, 2019), with most of them that apply fingerprinting techniques and/or clone sequencing. Actinobacteria and Proteobacteria have been generally reported as predominant within the freshwater sponge‐associated bacterial communities, whereas sequences affiliated to Bacteroidetes , Planctomycetes , Verrucomicrobia , Acidobacteria , and Armatimonadetes are often found at lower frequencies or seldom among dominant phyla.…”

“…The comparison of the bacterial communities residing in S. lacustris and other freshwater sponge species (e.g., B. intermedia , Corvospongilla lapidosa [Annandale, 1908], Ephydatia fluviatilis [Linneus, 1759], Eunapius carteri [Bowerbank, 1863], Lubomirskia baicalensis [Pallas, 1776], Swartschewskia papyracea [Dybowsky, 1880]) revealed certain taxonomic differences: Microbial sequences did not include phylotypes related to the phylum Verrucomicrobia ; Bacteroidota are generally reported among dominant phyla, whereas Acidobacteria are among less represented phyla, but this was not the case of S. lacustris ; Actinobacteria occurred, but they were not among the dominant phyla (Belikov et al, 2019; Clark et al, 2022; Costa et al, 2013; Gaikwad et al, 2016; Gernert et al, 2005; Kaluzhnaya et al, 2011; Kaluzhnaya & Itskovich, 2014, 2016; Kenny et al, 2019; Laport et al, 2019).…”

Effect of alkalinity and light intensity on the growth of the freshwater sponge Ephydatia fluviatilis (Porifera: Spongillidae)

“…Throughout the evolution toward to the freshwater environment, sponges from the family Spongillidae have followed adaptive paths peculiar to other representatives of their phylum, such as their ability to gemmulate in response to environmental adversity (Cáceres 1997). Further understanding of the underlying factors behind this peculiar phenomenon would allow determining to determine not only the ecological importance of modulating this quiescent state for these animals individually, but on the holobiont they comprise (Clark et al 2021).…”

Freshwater Sponges as a Neglected Reservoir of Bacterial Biodiversity

“…Two E. fragilis (Leidy, 1851) individuals were collected 1.5 km apart in the St. Lawrence River, North America [ 42 ]. A total of 851 isolates were obtained and identified as representatives of four major phyla commonly associated with sponges, i.e., Proteobacteria (including the genera Yersinia , Rahnella , Enterobacter , Pseudomonas , and Delftia ), Actinobacteria (genera Micromonospora , Verrucosispora , and Streptomyces ), Bacteroidetes (genus Chryseobacterium ), and Firmicutes (genera Bacillus and Paenibacillus ).…”