Predictable Changes in Eelgrass Microbiomes with Increasing Wasting Disease Prevalence across 23° Latitude in the Northeastern Pacific.

Predicting outcomes of marine disease outbreaks presents a challenge in the face of both global and local stressors. Host-associated microbiomes may play important roles in disease dynamics but remain understudied in marine ecosystems. Host-pathogen-microbiome interactions can vary across host ranges, gradients of disease, and temperature; studying these relationships may aid our ability to forecast disease dynamics. Eelgrass, Zostera marina, is impacted by outbreaks of wasting disease caused by the opportunistic pathogen Labyrinthula zosterae. We investigated how Z. marina phyllosphere microbial communities vary with rising wasting disease lesion prevalence and severity relative to plant and meadow characteristics like shoot density, longest leaf length, and temperature across 23° latitude in the Northeastern Pacific. We detected effects of geography (11%) and smaller, but distinct, effects of temperature (30-day max sea surface temperature, 4%) and disease (lesion prevalence, 3%) on microbiome composition. Declines in alpha diversity on asymptomatic tissue occurred with rising wasting disease prevalence within meadows. However, no change in microbiome variability (dispersion) was detected between asymptomatic and symptomatic tissues. Further, we identified members of Cellvibrionaceae, Colwelliaceae, and Granulosicoccaceae on asymptomatic tissue that are predictive of wasting disease prevalence across the geographic range (3,100 kilometers). Functional roles of Colwelliaceae and Granulosicoccaceae are not known. Cellvibrionaceae, degraders of plant cellulose, were also enriched in lesions and adjacent green tissue relative to nonlesioned leaves. Cellvibrionaceae may play important roles in disease progression by degrading host tissues or overwhelming plant immune responses. Thus, inclusion of microbiomes in wasting disease studies may improve our ability to understand variable rates of infection, disease progression, and plant survival. IMPORTANCE The roles of marine microbiomes in disease remain poorly understood due, in part, to the challenging nature of sampling at appropriate spatiotemporal scales and across natural gradients of disease throughout host ranges. This is especially true for marine vascular plants like eelgrass (Zostera marina) that are vital for ecosystem function and biodiversity but are susceptible to rapid decline and die-off from pathogens like eukaryotic slime-mold Labyrinthula zosterae (wasting disease). We link bacterial members of phyllosphere tissues to the prevalence of wasting disease across the broadest geographic range to date for a marine plant microbiome-disease study (3,100 km). We identify Cellvibrionaceae, plant cell wall degraders, enriched (up to 61% relative abundance) within lesion tissue, which suggests this group may be playing important roles in disease progression. These findings suggest inclusion of microbiomes in marine disease studies will improve our ability to predict ecological outcomes of infection across variable landscapes spanning thousands of kilometers.

The Future Is Big-and Small: Remote Sensing Enables Cross-Scale Comparisons of Microbiome Dynamics and Ecological Consequences.

Coupling remote sensing with microbial omics-based approaches provides a promising new frontier for scientists to scale microbial interactions across space and time. These data-rich, interdisciplinary methods allow us to better understand interactions between microbial communities and their environments and, in turn, their impact on ecosystem structure and function. Here, we highlight current and novel examples of applying remote sensing, machine learning, spatial statistics, and omics data approaches to marine, aquatic, and terrestrial systems. We emphasize the importance of integrating biochemical and spatiotemporal environmental data to move toward a predictive framework of microbiome interactions and their ecosystem-level effects. Finally, we emphasize lessons learned from our collaborative research with recommendations to foster productive and interdisciplinary teamwork.

Variable effects of local management on coral defenses against a thermally regulated bleaching pathogen.

Bleaching and disease are decimating coral reefs especially when warming promotes bleaching pathogens, such as Vibrio coralliilyticus. We demonstrate that sterilized washes from three common corals suppress V. coralliilyticus but that this defense is compromised when assays are run at higher temperatures. For a coral within the ecologically critical genus Acropora, inhibition was 75 to 154% greater among colonies from coral-dominated marine protected areas versus adjacent fished areas that were macroalgae-dominated. Acropora microbiomes were more variable within fished areas, suggesting that reef degradation may also perturb coral microbial communities. Defenses of a robust poritid coral and a weedy pocilloporid coral were not affected by reef degradation, and microbiomes were unaltered for these species. For some ecologically critical, but bleaching-susceptible, corals such as Acropora, local management to improve reef state may bolster coral resistance to global change, such as bacteria-induced coral bleaching during warming events.

Intergenerational effects of macroalgae on a reef coral: major declines in larval survival but subtle changes in microbiomes.

Tropical reefs are shifting from coral to macroalgal dominance, with macroalgae suppressing coral recovery, potentially via effects on coral microbiomes. Understanding how macroalgae affect corals and their microbiomes requires comparing algae- versus coral-dominated reefs without confounding aspects of time and geography. We compared survival, settlement, and post-settlement survival of larvae, as well as the microbiomes of larvae and adults, of the Pacific coral Pocillopora damicornis between an Marine Protected Area (MPA) dominated by corals versus an adjacent fished area dominated by macroalgae. Microbiome composition in adult coral, larval coral, and seawater did not differ between the MPA and fished area. However, microbiomes of adult coral were more variable in the fished area and Vibrionaceae bacteria, including strains most closely related to the pathogen Vibrio shilonii, were significantly enriched, but rare, in adult and larval coral from the fished area. Larvae from the macroalgae-dominated area exhibited higher pre-settlement mortality and reduced settlement compared to those from the coral-dominated area. Juveniles planted into a coral-dominated area survived better than those placed into a fished area dominated by macroalgae. Differential survival depended on whether macroalgae were immediately adjacent to juvenile coral rather than on traits of the areas per se. Contrary to our expectations, coral microbiomes were relatively uniform at the community level despite dramatic differences in macroalgal cover between the MPA (~2% cover) and fished (~90%) area. Reducing macroalgae may elicit declines in rare but potentially harmful microbes in coral and their larvae, as well as positive intergenerational effects on offspring survival.

Previously Uncultured Marine Bacteria Linked to Novel Alkaloid Production.

Low-nutrient media and long incubation times facilitated the cultivation of 20 taxonomically diverse Gram-negative marine bacteria within the phyla Bacteroidetes and Proteobacteria. These strains comprise as many as three new families and include members of clades that had only been observed using culture-independent techniques. Chemical studies of the type strains representing two new families within the order Cytophagales led to the isolation of nine new alkaloid secondary metabolites that can be grouped into four distinct structure classes, including azepinones, aziridines, quinolones, and pyrazinones. Several of these compounds possess antibacterial properties and appear, on structural grounds, to be produced by amino acid-based biosynthetic pathways. Our results demonstrate that relatively simple cultivation techniques can lead to the isolation of new bacterial taxa that are capable of the production of alkaloid secondary metabolites with antibacterial activities. These findings support continued investment in cultivation techniques as a method for natural product discovery.

Anthracimycin, a potent anthrax antibiotic from a marine-derived actinomycete.

Licensed to kill: A new antibiotic, anthracimycin (see scheme), produced by a marine-derived actinomycete in saline culture, shows significant activity toward Bacillus anthracis, the bacterial pathogen responsible for anthrax infections. Chlorination of anthracimycin gives a dichloro derivative that retains activity against Gram-positive bacteria, such as anthrax, but also shows activity against selected Gram-negative bacteria.

Mooreia alkaloidigena gen. nov., sp. nov. and Catalinimonas alkaloidigena gen. nov., sp. nov., alkaloid-producing marine bacteria in the proposed families Mooreiaceae fam. nov. and Catalimonadaceae fam. nov. in the phylum Bacteroidetes.

Bacterial strains CNX-216(T) and CNU-914(T) were isolated from marine sediment samples collected from Palmyra Atoll and off Catalina Island, respectively. Both strains were gram-negative and aerobic and produce deep-orange to pink colonies and alkaloid secondary metabolites. Cells of strain CNX-216(T) were short, non-motile rods, whereas cells of strain CNU-914(T) were short, curved rods with gliding motility. The DNA G+C contents of CNX-216(T) and CNU-914(T) were respectively 57.7 and 44.4 mol%. Strains CNX-216(T) and CNU-914(T) contained MK-7 as the predominant menaquinone and iso-C15 : 0 and C16 : 1ω5c as the major fatty acids. Phylogenetic analyses revealed that both strains belong to the order Cytophagales in the phylum Bacteroidetes. Strain CNX-216(T) exhibited low 16S rRNA gene sequence identity (87.1 %) to the nearest type strain, Cesiribacter roseus 311(T), and formed a well-supported lineage that is outside all currently described families in the order Cytophagales. Strain CNU-914(T) shared 97.6 % 16S rRNA gene sequence identity with 'Porifericola rhodea' N5EA6-3A2B and, together with 'Tunicatimonas pelagia' N5DB8-4 and four uncharacterized marine bacteria isolated as part of this study, formed a lineage that is clearly distinguished from other families in the order Cytophagales. Based on our polyphasic taxonomic characterization, we propose that strains CNX-216(T) and CNU-914(T) represent novel genera and species, for which we propose the names Mooreia alkaloidigena gen. nov., sp. nov. (type strain CNX-216(T)  = DSM 25187(T)  = KCCM 90102(T)) and Catalinimonas alkaloidigena gen. nov., sp. nov. (type strain CNU-914(T)  = DSM 25186(T)  = KCCM 90101(T)) within the new families Mooreiaceae fam. nov. and Catalimonadaceae fam. nov.