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The Redwood Microbiome: Microbial community composition and functional consequences of plant-microbe interactions for the tallest species on Earth

Abstract

The plant microbiome has proven to be an essential and often overlooked aspect of plant physiological ecology. Plant interactions with microbes are thought to have enabled the transition of plants from aquatic to terrestrial systems, thus co-evolving for millions of years. Consequently, microbes have important consequences for plant performance, nutrient cycling, and potentially even plant species ranges. However, our knowledge of these processes derives from only a few model systems. My dissertation explores these relationships in coast redwood forests where, despite their notoriety, plant-microbial relationships remain unexplored. Redwoods are the largest and some of the oldest plants on Earth, yet their geographical ranges are very constrained. As such, redwood forests serve as an excellent system to explore plant-microbial interactions and how they might expand or limit species ranges.

In Chapter 1, I demonstrate two unexpected and important findings related to the redwood root mycobiome. First, I show for the first time that, in addition to its expected association with arbuscular-mycorrhizal fungi (AMF), redwood roots are also associated with with ecto- and ericoid mycorrhizal fungi. To our knowledge, this is the first evidence that this predominantly AMF-associated tree is also colonized by the other two primary types of mycorrhizal fungi. These findings challenge the common practice of AMF-specific sequencing methods and the paradigm that plant species are assumed to associate with only one type of mycorrhizal fungi. This is important because it may link this tree species to the surrounding trees and shrubs that co-occur in these habitats. Secondly, I describe unique structures, which I call “rhizonodes”, that show many parallels in microbial community assembly to well-described nodules in N-fixing plants where rhizonodes act as reservoirs of AMF in the redwood roots. The presence of rhizonodes similarly are a unique finding that seem to occur in other predominantly AMF-associated tree species, but have been widely overlooked. We posit that these structures may be important domiciles for AMF in many of the upwards of 80% of plant species predicted to form relationships with this group. These findings also suggest that arbuscular mycorrhizal fungi (AMF) may play key roles in redwood physiology.

In Chapter 2, I focus on redwood association with AMF and the functional consequences of these interactions for plant hosts. I found that mycorrhization of coast redwood proceeds a number of downstream consequences for redwood hosts including in morphology, growth, allocation, hormonal physiology, drought-response, and leaf-level physiology. In addition, I found that mycorrhizal seedlings demonstrate progressively higher rates of photosynthesis compared to non-mycorrhizal seedlings in response to rising CO2. Together, these findings indicate that mycorrhizal fungi are likely to become increasingly important more broadly for plant response to climate change.

In Chapter 3, I demonstrate the importance of site-specific water-availability on the root-associated bacterial community in redwood. Previous work on crop plants has shown that artificial drought selects for monoderm bacteria, or bacterial taxa with a single, thick cell-wall layer. I present evidence of similar trends for a long-lived tree species in response to local water-availability. While the consequences of interactions with these types of bacteria remain unknown, as increased intensity and severity of drought are predicted as a result of climate change, I highlight the importance of testing the downstream consequences of monoderm versus diderm dominated bacterial communities on plant physiology, nutrient cycling, and ecosystem function.

Taken together, these studies suggest that the root microbiome is an important axis in understanding the response of redwood forest to climatic and environmental change predicted in the Anthropocene. Further, our study of a basal gymnosperm highlights important gaps in our understanding and categorization of plant-microbe interactions and emphasizes the importance of future investigations on non-model plant organisms.

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