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In recent years, it has become obvious that animal-microbe interactions play important roles in shaping ecosystems and human health. The Cleves Lab is broadly interested in the genetic and cellular mechanisms that underlie such interactions and how these interactions evolve. Specifically, we study the charismatic and ecologically important cnidarian-algal endosymbiosis (which is essential to the lives of reef-building corals) to explore these questions. We investigate this symbiosis with an integrated approach using both corals and a model system for coral biology, the symbiotic anemone Aiptasia.
In recent years, it has become obvious that animal-microbe interactions play important roles in shaping ecosystems and human health. The Cleves Lab is broadly interested in the genetic and cellular mechanisms that underlie such interactions and how these interactions are impacted by stress.
We study the charismatic and ecologically important symbiosis between coral and their intracellular algal symbionts. We focus on this particular symbiosis for two main reasons. First, it is a dramatic example of a beneficial endosymbiosis in animals. These types of interactions are poorly understood. Second, this symbiosis is critical for the survival of coral reefs, and its breakdown (or “coral bleaching”) due to anthropogenic stressors, including climate change, is leading to the global decline of coral ecosystems. The loss of these biodiversity hotspots is causing extensive economic and human health damage.
Despite the importance of this symbiosis, its molecular underpinnings are not well understood. This has been due primarily to the lack of tractable laboratory model systems and a lack of genetic tools. During the past several years, we have established genetic methods, such as morpholinos and CRISPR-Cas9, in both corals and a model system for coral biology, the symbiotic anemone Aiptasia. Our lab uses these new genetic tools and a combination of cellular, molecular, and developmental biology techniques to study symbiosis in both Aiptasia and reef-building corals.
Fig. 1: Integrated approach for understanding mechanisms underlying coral endosymbiosis and its breakdown. Strategy for using newly established genetic tools complemented by genomics and cell-biology approaches to elucidate the cnidarian-algal symbiosis.
RESEARCH INTERESTS:
1. What are the genetic and cellular pathways required to establish and maintain symbiosis?
Using a combination of ‘omics approaches, we have identified a set of genes and pathways potentially involved in the early steps of symbiosis formation and the maintenance of symbiosis. We are applying our novel genetic techniques to characterize the gene regulatory networks required for the symbiosis.
2. What genes and cellular mechanisms drive the breakdown of symbiosis due to stress? Despite hundreds of studies, we still do not understand the mechanisms that trigger and/or protect against bleaching. Several models have been proposed, but most have not been tested adequately. We are using a combination of genetic and cellular studies in Aiptasia and coral to investigate these mechanisms.
3. What underlies natural variation and evolution in the bleaching response?
Corals and anemones vary naturally in their tolerance to the stresses that cause bleaching. Major genetic contributors to this variation are both the cnidarians’ own genotypes and those of their algal symbionts. We are using model systems to discover how algal symbionts impact the ability of the host to tolerate stress.
4. Expand the genetic and molecular tool-kit for symbiotic cnidarians.
We are continuing to expand the number of state-of-the-art molecular techniques available in symbiotic cnidarians. These new tools will continue to facilitate the discovery of basic principles of symbiosis and animal-microbe interactions, broadly.
Unknown to Known: Advancing Knowledge of Coral Gene Function
PA Cleves, A Shumaker, JM Lee, HM Putnam, D Bhattacharya
Trends in Genetics 36 (2), 93-104
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2020 |
Varied effects of algal symbionts on transcription factor NF-κB in a sea anemone and a coral: possible roles in symbiosis and thermotolerance
KM Mansfield, PA Cleves, E Van Vlack, NG Kriefall, BE Benson, ...
bioRxiv, 640177
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2019 |
Strength in numbers: collaborative science for new experimental model systems
RF Waller, PA Cleves, M Rubio-Brotons, A Woods, SJ Bender, ...
PLoS biology 16 (7), e2006333
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2018 |
An intronic enhancer of Bmp6 underlies evolved tooth gain in sticklebacks
PA Cleves, JC Hart, RM Agoglia, MT Jimenez, PA Erickson, L Gai, ...
PLoS genetics 14 (6), e1007449
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2018 |
Genetic dissection of a supergene implicates Tfap2a in craniofacial evolution of threespine sticklebacks
PA Erickson, J Baek, JC Hart, PA Cleves, CT Miller
Genetics 209 (2), 591-605
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2018 |
CRISPR/Cas9-mediated genome editing in a reef-building coral
PA Cleves, ME Strader, LK Bay, JR Pringle, MV Matz
Proceedings of the National Academy of Sciences 115 (20), 5235-5240
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2018 |
Glucose-induced trophic shift in an endosymbiont dinoflagellate with physiological and molecular consequences
T Xiang, RE Jinkerson, S Clowez, C Tran, CJ Krediet, M Onishi, ...
Plant physiology 176 (2), 1793-1807
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2018 |
Transcription factor NF-κB is modulated by symbiotic status in a sea anemone model of cnidarian bleaching
KM Mansfield, NM Carter, L Nguyen, PA Cleves, A Alshanbayeva, ...
Scientific reports 7 (1), 1-14
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2017 |
Partially repeatable genetic basis of benthic adaptation in threespine sticklebacks
PA Erickson, AM Glazer, EE Killingbeck, RM Agoglia, J Baek, ...
Evolution 70 (4), 887-902
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2016 |
Distinct developmental genetic mechanisms underlie convergently evolved tooth gain in sticklebacks
NA Ellis, AM Glazer, NN Donde, PA Cleves, RM Agoglia, CT Miller
Development 142 (14), 2442-2451
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2015 |
A 190 base pair, TGF-β responsive tooth and fin enhancer is required for stickleback Bmp6 expression
PA Erickson, PA Cleves, NA Ellis, KT Schwalbach, JC Hart, CT Miller
Developmental biology 401 (2), 310-323
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2015 |
Parallel developmental genetic features underlie stickleback gill raker evolution
AM Glazer, PA Cleves, PA Erickson, AY Lam, CT Miller
Evodevo 5 (1), 19
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2014 |
Evolved tooth gain in sticklebacks is associated with a cis-regulatory allele of Bmp6
PA Cleves, NA Ellis, MT Jimenez, SM Nunez, D Schluter, DM Kingsley, ...
Proceedings of the National Academy of Sciences 111 (38), 13912-13917
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2014 |
Two developmentally temporal quantitative trait loci underlie convergent evolution of increased branchial bone length in sticklebacks
PA Erickson, AM Glazer, PA Cleves, AS Smith, CT Miller
Proceedings of the Royal Society B: Biological Sciences 281 (1788), 20140822
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2014 |
Congenital defects among liveborn infants with Down syndrome
MA Cleves, CA Hobbs, PA Cleves, JM Tilford, TM Bird, JM Robbins
Birth Defects Research Part A: Clinical and Molecular Teratology 79 (9), 657-663
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2007 |