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Biology subjects

Stachowicz, J. J.

Publications and source records attributed to Stachowicz, J. J..

8 recordsLinked to original sources

Distinct thermal responses of a host plant and an invertebrate herbivore affect ecosystem productivity and disease dynamics in a coastal marine ecosystem

Biological rates, like growth, tend to have unimodal (hump-shaped) responses to temperature, and these relationships can vary among species and biological processes. In most systems, full thermal performance relationships are rarely characterized for interacting species (e.g., consumer-resource or host-pathogen pairs), making it challenging to predict how their interactions, and subsequently, how communities, will shift with climate change. We investigated how the thermal responses of eelgrass (Zostera marina, an important marine foundation species in the N. hemisphere) and an isopod grazer (Pentidotea resecata), which putatively acts as an indirect vector of eelgrass wasting disease, interact to affect eelgrass productivity and wasting disease dynamics. In a laboratory experiment crossing five temperatures, two grazing, and two disease exposure treatments, across various metrics, eelgrass growth responded unimodally to temperature in the absence of grazers. Grazers depressed plant growth and flattened its thermal performance curves. Thermal performance curves for isopods indicated that increases in grazing and survival at intermediate temperatures negated concurrent gains in plant growth at these temperatures, while decreased isopod survival at high temperatures reduced their top-down effect on eelgrass. Isopods had negligible effects on plant disease responses, but warming reduced the time to disease onset and increased final disease severity. Overall, whole-plant disease severity remained low and did not substantially affect eelgrass leaf elongation, net growth, or rhizome dry mass. However, disease-treatment plants grew more new leaves at intermediate temperatures, possibly to combat losses in photosynthetic capacity in diseased leaf tissue. These results indicate that climate change-associated warming will likely increase eelgrass vulnerability to wasting disease. However, in sublethal outbreaks, disease could have less of an impact on eelgrass productivity than warming-induced increases in grazing. Thus, ignoring grazer responses to temperature could result in unreliable predictions of eelgrass productivity under climate change.

ecology↗

Seasonal differences in predation risk among seagrass epifauna species stabilize community-level predation over time

Predation risk varies through space and time due to changing refuge quality, predator communities, and prey traits. Despite this, ecological research is often focused on measuring average predation risk at the community level. While this can give important information about overall trophic transfer and ecological efficiency, it ignores differences in predation risk among prey species within a community, which may be important determinants of species coexistence and local diversity. We used crustaceans associated with temperate seagrass in Northern California to explore the relationship between seasonal variation in among-species and community-level predation risk for a community of morphologically distinct prey. We measured predation risk of the four most abundant and widespread prey species at six field sites every two to six weeks for one year. At the community level, sites differed significantly in their annual variation in predation risk, and these differences were correlated with the amount of variation in the among-species predation risk. When there was more within-year variation in predation risk among the four prey species, predation risk at the community level was more stable across the year. On the other hand, when each prey species in the community had similar levels of predation risk throughout the year, predation as a community-level process was much more seasonal and variable. Variation in predation risk also changed across a gradient of seagrass cover, a proxy for refuge quality. Sites with greater seagrass cover had less annual variation in community-level predation risk and more variation in predation risk among the four species at any given time point. In contrast, at sites with less eelgrass, all species were consumed at the same rate throughout the year, suggesting previously demonstrated differences in antipredator strategies among species are less relevant in the absence of habitat-forming species. We suggest that larger species-specific differences in predation risk throughout a year result in a more stable level of predation risk for the whole community, and that this may be driven by increased refuge provided by seagrass habitat mediating different prey species relative levels of susceptibility to predation.

ecology↗

Microbiome Assembly in Zostera marina during early host development: An EcoFAB 2.0 Application for Aquatic Plant-Microbe Interactions

Seagrass restoration practices are evolving to leverage microbiome applications, similar to agricultural systems that have demonstrated how targeted microbial communities enhance crop resilience in challenging environments. While adult seagrass microbiome research has expanded significantly, research on the seed microbiome remains critically understudied. This gap is particularly important given that seeds represent a large portion of restoration efforts. Advancing seed microbiome research requires standardized experimental systems for controlled plant-microbe interaction studies, which are currently lacking in seagrass research. Here, we tested fabricated ecosystem devices (EcoFAB 2.0) as a standardized system for growing seedlings of Zostera marina (eelgrass), enabling a controlled study of aquatic plant-microbe interactions. Using these chambers, we addressed three key questions: (i) Can we reliably grow eelgrass in a controlled laboratory setting? (ii) Can we manipulate eelgrass microbiome assembly and its long-term trajectory? and (iii) Can we detect shifts in the microbiome during plant development (host filtering)? Host morphology measurements and 16S rRNA gene amplicon sequencing were used to track microbiome assembly across three early developmental stages of the host. We identified 143 ASVs that differed between plants from surface-sterilized versus intact seeds, highlighting the strong influence of epiphytic bacteria on microbiome assembly. We also identified 26 stage-specific indicator ASVs across eelgrass development, suggesting stage-specific microbial associations during seedling establishment. This work demonstrates the potential for targeted manipulation of the microbiome in seagrass for restoration efforts. ImportanceUsing the Fabricated Ecosystem 2.0 (EcoFAB 2.0), we were able to successfully control the microbial environment of Z. marina, resulting in the removal of epiphytes and maintaining low microbial diversity across plants without compromising the growth dynamics of the seedlings. Our findings advance the marine plant model system, Zostera marina, by identifying taxonomic indicators across life stages. This work lays the foundation for a targeted understanding and application of microbiomes for seagrass restoration, bridging the critical knowledge gap between agricultural seed microbiome success and marine restoration applications.

microbiology↗

Low-pH conditions drive transient changes in shell calcification and the microbiome in a pH-resistant strain of the the Pacific oyster Magallana gigas

The study explores the effects of elevated pCO2 on shell calcification, microbiome composition, and gene expression in a strain of Pacific oyster (Magallana gigas) selectively bred for low-pH resistance. Juvenile oysters reared under low-pH conditions exhibited increased shell mass compared to the control population by 51 days post-fertilization, despite high variance in shell size at earlier stages. Microbiome analyses revealed significant shifts in community composition under low-pH conditions, particularly in bacterial taxa involved in CO2 production and biogeochemical cycling, which could influence carbonate chemistry within oyster tissues. Gene expression profiling demonstrates differential regulation of genes related to biomineralization, immunity, and microbial interactions under low-pH conditions. For example, multiple carbonic anhydrases exhibited treatment-specific expression patterns, suggesting a role in adapting to low-pH environments. Observed changes in immune-related genes imply a relaxation of immune responses, potentially reflecting resource reallocation toward calcification processes. These results collectively support the "dysbiosis hypothesis," where oysters adapt to environmental stress by modulating their microbiomes and gene expression. Future studies should investigate whether these responses are consistent across oyster strains and environmental conditions, providing insights into the resilience of aquaculture species to ocean acidification. SUMMARY STATEMENTElevated pCO2 impacts Pacific oyster calcification, microbiome composition, and gene expression, suggesting genetic adaptation and microbiome shifts may be crucial for resilience to ocean acidification.

systems biology↗

Ocean currents drive the worldwide colonization of the most widespread marine plant, eelgrass (Zostera marina)

Currents are unique drivers of oceanic phylogeography and so determine the distribution of marine coastal species, along with past glaciations and sea level changes. Here, we reconstruct the worldwide colonization history of eelgrass (Zostera marina L.), the most widely distributed marine flowering plant or seagrass from its origin in the Northwest Pacific, based on nuclear and chloroplast genomes. We identified two divergent Pacific clades with evidence for admixture along the East Pacific coast. Multiple west to east (trans-Pacific) colonization events support the key role of the North Pacific Current. Time-calibrated nuclear and chloroplast phylogenies yielded concordant estimates of the arrival of Z. marina in the Atlantic through the Canadian Arctic, suggesting that eelgrass-based ecosystems, hotspots of biodiversity and carbon sequestration, have only been present since [~]208 Kya (thousand years ago). Mediterranean populations were founded [~]53 Kya while extant distributions along western and eastern Atlantic shores coincide with the end of the Last Glacial Maximum ([~]20 Kya). The recent colonization and 5-to 7-fold lower genomic diversity of Atlantic compared to the Pacific populations raises concern and opportunity about how Atlantic eelgrass might respond to rapidly warming coastal oceans.

evolutionary biology↗

Using "identity by heterozygosity (IBH)" to detect clonemates under prevalent clonal reproduction in multicellular diploids

Clonal reproduction, the formation of new individuals that are genetically nearly identical to the parent via mitosis in the absence of genetic recombination, is a very common reproductive mode across plants, fungi, and animals. Current genetic marker based methods fail to detect clonal structure when all collected samples belong to one single clone, which seems to be more common than previously thought. Here we propose a new similarity index, "Shared Heterozygosity (SH)" based on the number of genetic markers (typically SNPs, single-nucleotide polymorphisms) that are identically heterozygous among two or more genomes (i.e., NSH). Ideally NSH should be on the order of approximately >=3,000, which can be easily achieved nowadays via Restriction-site Associated DNA (RAD) sequencing or whole-genome resequencing. One should be careful when NSH is small (roughly <1,000). We analyze two large seagrass clones (Posidonia australis, Zostera marina) along with two Z. marina clones of known age (17-yrs), and show that SH can potentially extend the detection of clonemates to any pair of samples with the aid of technical replicates. Another potential application of SH is to detect possible parent-descendant pairs under selfing, because the heterozygous loci in the selfing-produced descendants represent a subset of those in the parent. Our proposed workflow takes advantage of the availability of the larger number of genetic markers in the genomic era, and fills a gap in detecting clonemates in the growing number of cases where many or all samples at a location belong to one single clone.

evolutionary biology↗

More than a stick in the mud: Eelgrass leaf and root bacterial communities are distinct from those on physical mimics

We examine the role of physical structure vs. biotic interactions in structuring host-associated microbial communities on a marine angiosperm, Zostera marina, eelgrass. Across several months and sites, we compared microbiomes on physical mimics of eelgrass roots and leaves to those on intact plants. We find large, consistent differences in the microbiome of mimics and plants, especially on roots, but also on leaves. Key taxa that are more abundant on leaves have been associated with microalgal and macroalgal disease and merit further investigation to determine their role in mediating plant-microalgal-pathogen interactions. Root associated taxa were associated with sulfur and nitrogen cycling, potentially ameliorating environmental stresses for the plant. Our work identifies targets for future work on the functional role of the seagrass microbiome in promoting the success of these angiosperms in the sea. Originality-Significance StatementWe show that eelgrass establishes a distinct microbial community from a physical mimic on both its leaves and roots. This is, to our knowledge, the first comparison of seagrass to a mimicked physical environment. Insights from our study establish bacterial targets for future functional studies of seagrass-microbiome interactions.

ecology↗

Global-scale structure of the eelgrass microbiome

Plant-associated microorganisms are essential for their hosts' survival and performance. Yet, most plant microbiome studies to date have focused on terrestrial plant species sampled across relatively small spatial scales. Here we report results of a global-scale analysis of microbial communities associated with leaf and root surfaces of the marine eelgrass Zostera marina throughout its range in the Northern Hemisphere. By contrasting host microbiomes with those of their surrounding seawater and sediment communities, we uncovered the structure, composition and variability of microbial communities associated with Z. marina. We also investigated hypotheses about the mechanisms driving assembly of the eelgrass microbiome using a whole-genomic metabolic modeling approach. Our results reveal aboveground leaf communities displaying high variability and spatial turnover, that strongly mirror their adjacent coastal seawater microbiomes. In contrast, roots showed relatively low spatial turnover and were compositionally distinct from surrounding sediment communities -- a result largely driven by the enrichment of predicted sulfur-oxidizing bacterial taxa on root surfaces. Metabolic modeling of enriched taxa was consistent with an assembly process whereby similarity in resource use drives taxonomic co-occurrence patterns on belowground, but not aboveground, host tissues. Our work provides evidence for a core Z. marina root microbiome with putative functional roles and highlights potentially disparate processes influencing microbiome assembly on different plant compartments.

microbiology↗