Year of Award

2023

Document Type

Dissertation

Degree Type

Doctor of Philosophy (PhD)

Degree Name

Organismal Biology, Ecology, and Evolution

Other Degree Name/Area of Focus

Ecology and Evolution

Department or School/College

Division of Biological Sciences

Committee Chair

Scott R. Miller

Commitee Members

Mathew Church, Lila Fishman, Anna Sala, Patrick Secor, Art Woods

Abstract

The origin of novel traits is an important evolutionary process that generates biological diversity. However, we rarely know the underlying mechanisms of diversification following the innovation of a novel trait. Over two billion years ago, the innovation of chlorophyll (Chl) abased photosynthesis by cyanobacteria sparked the oxygenation of Earth, setting the stage for the emergence of multicellular life. Chl a was subsequently acquired by diverse algae and plants, and in the process, these organisms diversified their light-harvesting systems to absorb a range of visible wavelengths (400-700 nm) (1). Due to the ancient origins of Chl a, however, it is difficult to reconstruct diversification of these light-harvesting systems. By contrast, the comparatively recent invention of Chl d (~10-100 million years ago) by the cyanobacterium Acaryochloris marina (2) enables us to examine the process of diversification following the invention of a novel Chl pigment. In A. marina, Chl d is the major photosynthetic pigment, which shifts the pigment absorption into far-red, low-energy photons (700-750 nm). Despite A. marina’s wide distribution in shallow saline environments, the evolution and diversification of its unique light-harvesting system is not understood.

In my dissertation, I use the A. marina system to investigate the consequences of novel trait innovation. In Chapter 1, I introduce our A. marina culture collection consisting of 54 laboratory strains and genome resources. In Chapter 2, I document an extraordinary burst of diversification of A. marina’s light-harvesting system composition and function. These changes have altered the kinds of far-red photons that are preferentially used by A. marina. I conclude that the innovation of Chl d was quickly followed by diversification, which enabled A. marina to fill new ecological niches. In Chapter 3, I investigate the origin and ecological consequences of the phycobiliprotein light-harvesting structure that was identified in A. marina strain MBIC11017 (3). Unlike most cyanobacteria, the ability to produce pigments called phycobiliproteins that harvest visible light was lost by the A. marina ancestor. I report that MBIC11017 has recently regained the genes required to make the phycobiliprotein phycocyanin (PC) via horizontal gene transfer from a distant relative, enabling it to grow in visible light otherwise inaccessible to other A. marina strains (4). I build on this in Chapter 4 by examining how existing gene regulatory networks are re-wired to accommodate novel traits. Using a comparative transcriptomic approach between MBIC11017 and its PC-lacking close relative MU13, I investigate potential mechanisms of PC regulatory assimilation. I report that PC assembly and degradation processes have been reassimilated into a conserved ancestral response to high light.

Taken together, my dissertation establishes the unique A. marina system as a model for extending far-red oxygenic photosynthesis to agricultural and biotechnological systems. In addition to these chapters, I contributed to several other related projects: peer-reviewed research articles on the genomic and functional variation of A. marina (5) and adaptation by expansion of insertion sequence elements in A. marina (6). Collectively, my dissertation and related projects contribute groundbreaking insights into fundamental evolutionary biology questions of how novel traits evolve and impact biological diversification.

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