A comprehensive analysis of the microbial communities of healthy and diseased marine macroalgae and the detection of known and potential bacterial pathogens

Abstract

Microorganisms are increasingly being recognized as the causative agents in the diseases of marine higher organisms, such as corals, sponges, and macroalgae. Delisea pulchra is a common, temperate red macroalga, which suffers from a bleaching disease. Two bacterial strains, Nautella italica R11 and Phaeobacter gallaeciensis LSS9, have been shown in vitro to cause bleaching symptoms, but previous work has failed to detect them during a natural bleaching event. To provide a link between in vitro observations and natural occurrences of the disease, we employ here deep-sequencing of the 16S rRNA gene to comprehensively analyze the community composition of healthy and diseased D. pulchra samples from two separate locations. We observed operational taxonomic units (OTUs) with 100% identity and coverage to the 16S RNA gene sequence of both in vitro pathogens, but only the OTU with similarity to strain LSS9 showed a statistically significant higher abundance in diseased samples. Our analysis also reveals the existence of other bacterial groups within the families Rhodobacteraceae and Flavobacteriaceae that strongly contribute to difference between diseased and healthy samples and thus these groups potentially contain novel macroalgal pathogens and/or saprophytes. Together our results provide evidence for the ecological relevance of one kind of in vitro pathogen, but also highlight the possibility that multiple opportunistic pathogens are involved in the bleaching disease of D. pulchra.

Microbial community function in the bleaching disease of the marine macroalgae Delisea pulchra

“…Twenty‐six out of the 231 OTUs of the present study matched (with 100% identity and subject coverage cutoffs) to OTUs from a previous study analysing D. pulchra 's communities by 16S rRNA gene amplicon sequencing (Zozaya‐Valdes et al ., ) (Supporting Information Table S5). Of these, one OTU (i.e.…”

“…Some bins could be classified at lower taxonomic levels and three belonged to the Rhodobacteraceae , Rhodobacterales and Verrumicrobiales (Supporting Information Table S9). Previously, OTUs belonging to these taxa have been found enriched in bleached D. pulchra (Fernandes et al ., ; Zozaya‐Valdes et al ., ).…”

“…and Supporting Information Fig. S1), similar to what has been seen previously based on 16S rRNA gene amplicon data (Fernandes et al ., ; Zozaya‐Valdes et al ., ). Three bacterial families ( Rhodobacteriaceae , Saprospiraceae and Flavobacteriaceae ) were consistently enriched across these studies, as was an OTU corresponding to the recently identified Aquimarina sp.…”

“…pathogen (Kumar et al ., ). However, the majority of OTUs significantly enriched in bleached samples of the present and previous work (Zozaya‐Valdes et al ., ) were different. While the different methodological approaches used in these studies could explain this difference, high variability of bleaching‐enriched OTUs was also seen between individuals within the same study (Supporting Information Fig.…”

Incubation with macroalgae induces large shifts in water column microbiota, but minor changes to the epibiota of co‐occurring macroalgae

“…Some microbes provide benefits for their macroalgal hosts by improving nutrient acquisition (Chisholm, Douga, Ageron, Grimont, & Jaubert, ; Croft, Lawrence, Raux‐Deery, Warren, & Smith, ; Ilead & Carpenter, ; Rosenberg & Paerl, ), promoting settlement and growth (Joint et al., ) and priming immune responses against potential pathogens (Armstrong, Yan, Boyd, Wright, & Burgess, ; Dobretsov & Qian, ; Küpper, Müller, Peters, Kloareg, & Potin, ; Maximilian et al., ; Steinberg, Schneider, & Kjelleberg, ; Weinberger, ). Other microbes, however, cause tissue bleaching (Case et al., ; Zozaya‐Valdes, Egan, & Thomas, ) and initiate or exasperate tissue degradation (Egan et al., ; Küpper et al., ). It is important to understand the assembly of macroalgal microbiota to gain insight into the factors that promote establishment and growth of beneficial or pathogenic microbes.…”