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

   https://doi.org/10.1128/msystems.00224-22  

   Beatty, Deanna S. ; Aoki, Lillian R. ; Rappazzo, Brendan ; Bergman, Chelsea ; Domke, Lia K. ; Duffy, J. Emmett ; Dubois, Katie ; Eckert, Ginny L. ; Gomes, Carla ; Graham, Olivia J. ; et al ( August 2022 , mSystems)

   Raina, Jean-Baptiste (Ed.)

   ABSTRACT 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. 

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2. An inverse latitudinal gradient in infection probability and phylogenetic diversity for Leucocytozoon blood parasites in New World birds

   https://doi.org/10.1111/1365-2656.13117  

   Fecchio, Alan ; Bell, Jeffrey A. ; Bosholn, Mariane ; Vaughan, Jefferson A. ; Tkach, Vasyl V. ; Lutz, Holly L. ; Cueto, Victor R. ; Gorosito, Cristian A. ; González‐Acuña, Daniel ; Stromlund, Chad ; et al ( October 2019 , Journal of Animal Ecology)

   Geographic variation in environmental conditions as well as host traits that promote parasite transmission may impact infection rates and community assembly of vector‐transmitted parasites.

   Identifying the ecological, environmental and historical determinants of parasite distributions and diversity is therefore necessary to understand disease outbreaks under changing environments. Here, we identified the predictors and contributions of infection probability and phylogenetic diversity ofLeucocytozoon(an avian blood parasite) at site and species levels across the New World.

   To explore spatial patterns in infection probability and lineage diversity forLeucocytozoonparasites, we surveyed 69 bird communities from Alaska to Patagonia. Using phylogenetic Bayesian hierarchical models and high‐resolution satellite remote‐sensing data, we determined the relative influence of climate, landscape, geography and host phylogeny on regional parasite community assembly.

   Infection rates and parasite diversity exhibited considerable variation across regions in the Americas. In opposition to the latitudinal gradient hypothesis, both the diversity and prevalence ofLeucocytozoonparasites decreased towards the equator. Host relatedness and traits known to promote vector exposure neither predicted infection probability nor parasite diversity. Instead, the probability of a bird being infected withLeucocytozoonincreased with increasing vegetation cover (NDVI) and moisture levels (NDWI), whereas the diversity of parasite lineages decreased with increasing NDVI. Infection rates and parasite diversity also tended to be higher in cooler regions and higher latitudes.

   Whereas temperature partially constrainsLeucocytozoondiversity and infection rates, landscape features, such as vegetation cover and water body availability, play a significant role in modulating the probability of a bird being infected. This suggests that, forLeucocytozoon, the barriers to host shifting and parasite host range expansion are jointly determined by environmental filtering and landscape, but not by host phylogeny. Our results show that integrating host traits, host ancestry, bioclimatic data and microhabitat characteristics that are important for vector reproduction are imperative to understand and predict infection prevalence and diversity of vector‐transmitted parasites. Unlike other vector‐transmitted diseases, our results show thatLeucocytozoondiversity and prevalence will likely decrease with warming temperatures.

    

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3. Global drivers of avian haemosporidian infections vary across zoogeographical regions

   https://doi.org/10.1111/geb.13390  

   Fecchio, Alan ; Clark, Nicholas J. ; Bell, Jeffrey A. ; Skeen, Heather R. ; Lutz, Holly L. ; De La Torre, Gabriel M. ; Vaughan, Jefferson A. ; Tkach, Vasyl V. ; Schunck, Fabio ; Ferreira, Francisco C. ; et al ( September 2021 , Global Ecology and Biogeography)

   Macroecological analyses provide valuable insights into factors that influence how parasites are distributed across space and among hosts. Amid large uncertainties that arise when generalizing from local and regional findings, hierarchical approaches applied to global datasets are required to determine whether drivers of parasite infection patterns vary across scales. We assessed global patterns of haemosporidian infections across a broad diversity of avian host clades and zoogeographical realms to depict hotspots of prevalence and to identify possible underlying drivers.

   Global.

   1994–2019.

   Avian haemosporidian parasites (generaPlasmodium,Haemoproteus,LeucocytozoonandParahaemoproteus).

   We amalgamated infection data from 53,669 individual birds representing 2,445 species world‐wide. Spatio‐phylogenetic hierarchical Bayesian models were built to disentangle potential landscape, climatic and biotic drivers of infection probability while accounting for spatial context and avian host phylogenetic relationships.

   Idiosyncratic responses of the three most common haemosporidian genera to climate, habitat, host relatedness and host ecological traits indicated marked variation in host infection rates from local to global scales. Notably, host ecological drivers, such as migration distance forPlasmodiumandParahaemoproteus, exhibited predominantly varying or even opposite effects on infection rates across regions, whereas climatic effects on infection rates were more consistent across realms. Moreover, infections in some low‐prevalence realms were disproportionately concentrated in a few local hotspots, suggesting that regional‐scale variation in habitat and microclimate might influence transmission, in addition to global drivers.

   Our hierarchical global analysis supports regional‐scale findings showing the synergistic effects of landscape, climate and host ecological traits on parasite transmission for a cosmopolitan and diverse group of avian parasites. Our results underscore the need to account for such interactions, in addition to possible variation in drivers across regions, to produce the robust inference required to predict changes in infection risk under future scenarios.

    

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4. Temperature dependence of parasitic infection and gut bacterial communities in bumble bees

   https://doi.org/10.1111/1462-2920.14805  

   Palmer‐Young, Evan C. ; Ngor, Lyna ; Burciaga Nevarez, Rodrigo ; Rothman, Jason A. ; Raffel, Thomas R. ; McFrederick, Quinn S. ( November 2019 , Environmental Microbiology)

   High temperatures (e.g., fever) and gut microbiota can both influence host resistance to infection. However, effects of temperature‐driven changes in gut microbiota on resistance to parasites remain unexplored. We examined the temperature dependence of infection and gut bacterial communities in bumble bees infected with the trypanosomatid parasiteCrithidia bombi. Infection intensity decreased by over 80% between 21 and 37°C. Temperatures of peak infection were lower than predicted based on parasite growthin vitro, consistent with mismatches in thermal performance curves of hosts, parasites and gut symbionts. Gut bacterial community size and composition exhibited slight but significant, non‐linear, and taxon‐specific responses to temperature. Abundance of total gut bacteria and of Orbaceae, both negatively correlated with infection in previous studies, were positively correlated with infection here. Prevalence of the bee pathogen‐containing family Enterobacteriaceae declined with temperature, suggesting that high temperature may confer protection against diverse gut pathogens. Our results indicate that resistance to infection reflects not only the temperature dependence of host and parasite performance, but also temperature‐dependent activity of gut bacteria. The thermal ecology of gut parasite‐symbiont interactions may be broadly relevant to infectious disease, both in ectothermic organisms that inhabit changing climates, and in endotherms that exhibit fever‐based immunity.

    

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5. Effects of Seagrass Wasting Disease on Eelgrass Growth and Belowground Sugar in Natural Meadows

   https://doi.org/10.3389/fmars.2021.768668  

   Graham, Olivia J. ; Aoki, Lillian R. ; Stephens, Tiffany ; Stokes, Joshua ; Dayal, Sukanya ; Rappazzo, Brendan ; Gomes, Carla P. ; Harvell, C. Drew ( November 2021 , Frontiers in Marine Science)

   Seagrass meadows provide valuable ecosystem benefits but are at risk from disease. Eelgrass ( Zostera marina ) is a temperate species threatened by seagrass wasting disease (SWD), caused by the protist Labyrinthula zosterae . The pathogen is sensitive to warming ocean temperatures, prompting a need for greater understanding of the impacts on host health under climate change. Previous work demonstrates pathogen cultures grow faster under warmer laboratory conditions and documents positive correlations between warmer ocean temperatures and disease levels in nature. However, the consequences of disease outbreaks on eelgrass growth remain poorly understood. Here, we examined the effect of disease on eelgrass productivity in the field. We coupled in situ shoot marking with high-resolution imagery of eelgrass blades and used an artificial intelligence application to determine disease prevalence and severity from digital images. Comparisons of eelgrass growth and disease metrics showed that SWD impaired eelgrass growth and accumulation of non-structural carbon in the field. Blades with more severe disease had reduced growth rates, indicating that disease severity can limit plant growth. Disease severity and rhizome sugar content were also inversely related, suggesting that disease reduced belowground carbon accumulation. Finally, repeated measurements of diseased blades indicated that lesions can grow faster than healthy tissue in situ . This is the first study to demonstrate the negative impact of wasting disease on eelgrass health in a natural meadow. These results emphasize the importance of considering disease alongside other stressors to better predict the health and functioning of seagrass meadows in the Anthropocene. 

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