Differential Response of Bacterial Microdiversity to Simulated Global Change

ACKNOWLEDGMENTS UC Irvine and the LRGCE are located on the ancestral homelands of the Indigenous Kizh and Acjachemen nations. We thank Alejandra Rodriguez Verdugo, Katrine Whiteson, Kendra Walters, Cynthia Rodriguez, Kristin Barbour, Alberto Barron Sandoval, Joanna Wang, Joia Kai Capocchi, Pauline Uyen Phuong Nguyen, Khanh Thuy Huynh, and Clara Barnosky for their input on analyses and previous drafts and for laboratory help. This work was supported by the U.S. Department of Energy, Office of Science, Office of Biological and Environmental Research grants DE-SC0016410 and DE-SC0020382.Peer reviewedPublisher PD

Environmental Shaping of Sponge Associated Archaeal Communities

Archaea are ubiquitous symbionts of marine sponges but their ecological roles and the influence of environmental factors on these associations are still poorly understood.We compared the diversity and composition of archaea associated with seawater and with the sponges Hymeniacidon heliophila, Paraleucilla magna and Petromica citrina in two distinct environments: Guanabara Bay, a highly impacted estuary in Rio de Janeiro, Brazil, and the nearby Cagarras Archipelago. For this we used metagenomic analyses of 16S rRNA and ammonia monooxygenase (amoA) gene libraries. Hymeniacidon heliophila was more abundant inside the bay, while P. magna was more abundant outside and P. citrina was only recorded at the Cagarras Archipelago. Principal Component Analysis plots (PCA) generated using pairwise unweighted UniFrac distances showed that the archaeal community structure of inner bay seawater and sponges was different from that of coastal Cagarras Archipelago. Rarefaction analyses showed that inner bay archaeaoplankton were more diverse than those from the Cagarras Archipelago. Only members of Crenarchaeota were found in sponge libraries, while in seawater both Crenarchaeota and Euryarchaeota were observed. Although most amoA archaeal genes detected in this study seem to be novel, some clones were affiliated to known ammonia oxidizers such as Nitrosopumilus maritimus and Cenarchaeum symbiosum.The composition and diversity of archaeal communities associated with pollution-tolerant sponge species can change in a range of few kilometers, probably influenced by eutrophication. The presence of archaeal amoA genes in Porifera suggests that Archaea are involved in the nitrogen cycle within the sponge holobiont, possibly increasing its resistance to anthropogenic impacts. The higher diversity of Crenarchaeota in the polluted area suggests that some marine sponges are able to change the composition of their associated archaeal communities, thereby improving their fitness in impacted environments

Ecological and evolutionary consequences of microbial community responses to environmental change

Global changes such as increased frequency of fire, drought, and nitrogen deposition, perturb microorganisms and the higher trophic life forms they support. Microorganisms play key roles in carbon and nutrient cycling, which are important to agriculture and ecosystem health. Although microorganisms are pivotal in an ecosystem's response to environmental changes, little is known about how abundant and diverse microbial communities adapt to such changes. The overarching aim of my thesis is to investigate how bacterial communities respond to global change and in particular, their ability to quickly adapt to environmental perturbations. I first investigated how microbial responses to global changes are influenced by interactions with plant communities using the Loma Ridge Global Change Experiment, a decade-long experiment that manipulates rainfall and nitrogen levels across two adjacent ecosystems (Chapter 1). My findings underscore the importance of plant–microbe interactions when considering the transferability of the results of global change experiments across ecosystems. Next, I investigated traits found on plasmids, a type of mobile genetic element (MGE) that can facilitate rapid evolution in bacteria. I asked what are the ecologically-relevant plasmid genes that may serve as reservoirs of environmental-adaptive traits in bacteria (Chapter 2). The findings of this chapter suggest that plasmid traits may contribute to host adaptation in environmental microbiomes. Lastly, I extended this work to a cosmopolitan soil taxon, Curtobacterium, an abundant genus of bacteria in southern California ecosystems. This taxon shows marked shifts in relative abundance in response to simulated drought and is amenable to culturing, providing a tractable system for investigating both genotypic and phenotypic characteristics of this organism. Previous experiments have shown Curtobacterium rapidly evolve via de novo mutations in response to environmental changes. I asked what MGE and associated traits are found in Curtobacterium, and determined whether MGE and traits showed any environment- versus clade- specific genomic signatures (Chapter 3). The findings of this chapter highlight the potential of traits found on plasmids to be mobilized within the bacterial communities where these Curtobacterium were isolated. Overall, my thesis work highlights the importance for considering the intersection of evolution and ecology in understanding how microbial communities adapt to environmental changes

Microbial community response to a decade of simulated global changes depends on the plant community

Global changes such as increased drought and atmospheric nitrogen deposition perturb both the microbial and plant communities that mediate terrestrial ecosystem functioning. However, few studies consider how microbial responses to global changes may be influenced by interactions with plant communities. To begin to address the role of microbial–plant interactions, we tested the hypothesis that the response of microbial communities to global change depends on the plant community. We characterized bacterial and fungal communities from 395 plant litter samples taken from the Loma Ridge Global Change Experiment, a decade-long global change experiment in Southern California that manipulates rainfall and nitrogen levels across two adjacent ecosystems, a grassland and a coastal sage scrubland. The differences in bacterial and fungal composition between ecosystems paralleled distinctions in plant community composition. In addition to the direct main effects, the global change treatments altered microbial composition in an ecosystem-dependent manner, in support of our hypothesis. The interaction between the drought treatment and ecosystem explained nearly 5% of the variation in bacterial community composition, similar to the variation explained by the ecosystem-independent effects of drought. Unexpectedly, we found that the main effect of drought was approximately four times as strong on bacterial composition as that of nitrogen addition, which did not alter fungal or plant composition. Overall, the findings underscore the importance of considering plant–microbe interactions when considering the transferability of the results of global change experiments across ecosystems