Genomics of Sponge-Associated Streptomyces spp. Closely Related to Streptomyces albus J1074: Insights into Marine Adaptation and Secondary Metabolite Biosynthesis Potential

Abstract

A total of 74 actinomycete isolates were cultivated from two marine sponges, Geodia barretti and Phakellia ventilabrum collected at the same spot at the bottom of the Trondheim fjord (Norway). Phylogenetic analyses of sponge-associated actinomycetes based on the 16S rRNA gene sequences demonstrated the presence of species belonging to the genera Streptomyces, Nocardiopsis, Rhodococcus, Pseudonocardia and Micromonospora. Most isolates required sea water for growth, suggesting them being adapted to the marine environment. Phylogenetic analysis of Streptomyces spp. revealed two isolates that originated from different sponges and had 99.7% identity in their 16S rRNA gene sequences, indicating that they represent very closely related strains. Sequencing, annotation, and analyses of the genomes of these Streptomyces isolates demonstrated that they are sister organisms closely related to terrestrial Streptomyces albus J1074. Unlike S. albus J1074, the two sponge streptomycetes grew and differentiated faster on the medium containing sea water. Comparative genomics revealed several genes presumably responsible for partial marine adaptation of these isolates. Genome mining targeted to secondary metabolite biosynthesis gene clusters identified several of those, which were not present in S. albus J1074, and likely to have been retained from a common ancestor, or acquired from other actinomycetes. Certain genes and gene clusters were shown to be differentially acquired or lost, supporting the hypothesis of divergent evolution of the two Streptomyces species in different sponge hosts.

Evaluation of antagonistic activities against Pythium myriotylum and plant growth promoting traits of Streptomyces isolated from Cocoyam (Xanthosoma sagittifolium (L.) Schott) rhizosphere

“…S. albulus are known for their ability to produce Ɛ-polylysine, which exhibits antimicrobial activity against yeast, fungi and bacteria (Yoshida et al, 2003;Jianjun et al, 2012;Wu et al, 2015). S. albus has been isolated from diverse environments including sponges, sea sediments and insects and have been reported as biocontrol agents against fruit and vegetable pathogens (Ian et al, 2014;Hanshew et al, 2014). Analysis of extracts derived from Streptomyces gandocaensis strain, which was isolated from marine sediment in Costa Rica, resulted in the discovery of an antibiotics cahuitamycins, new inhibitors of biofilm formation (Park et al, 2016).…”

Recent advances in understanding Streptomyces

“…within a species group). Ten biosynthetic gene clusters were specific to, and conserved among, the J1074 group, while a roughly equal number showed some degree of isolate specificity 33, 47 .…”

“…In a further illustration of the ecological diversity of streptomycetes, strains adapted to marine conditions are prominent in the microbiota of marine sponges 33 .…”

“…Generally, comparative genomics of closely related streptomycetes has had little attention, though marine isolates from two distinct sponges were interestingly closely related to the terrestrial Streptomyces albus G derivative J1074 (which is often used for heterologous expression work) in a study identifying candidate marine-adaptation genes present only in the two marine isolates and in some other marine actinomycetes 33, 47 . Four further J1074-related organisms were subsequently found in 140 Streptomyces genomes available at the time, making this species group the most readily isolated to date 33, 47 .…”

“…Four further J1074-related organisms were subsequently found in 140 Streptomyces genomes available at the time, making this species group the most readily isolated to date 33, 47 . This provided an opportunity to examine the dynamics of acquisition and loss of secondary metabolite biosynthetic gene sets in relatively recent evolution (i.e.…”