Wong and Hofmann BMC Genomics (2021) 22:32 https://doi.org/10.1186/s12864-020-07327-x RESEARCH ARTICLE Open Access Gene expression patterns of red sea urchins (Mesocentrotus franciscanus) exposed to different combinations of temperature and pCO2 during early development Juliet M. Wong1,2* and Gretchen E. Hofmann1 Abstract Background: The red sea urchin Mesocentrotus franciscanus is an ecologically important kelp forest herbivore and an economically valuable wild fishery species. To examine how M. franciscanus responds to its environment on a molecular level, differences in gene expression patterns were observed in embryos raised under combinations of two temperatures (13 °C or 17 °C) and two pCO2 levels (475 μatm or 1050 μatm). These combinations mimic various present-day conditions measured during and between upwelling events in the highly dynamic California Current System with the exception of the 17 °C and 1050 μatm combination, which does not currently occur. However, as ocean warming and acidification continues, warmer temperatures and higher pCO2 conditions are expected to increase in frequency and to occur simultaneously. The transcriptomic responses of the embryos were assessed at two developmental stages (gastrula and prism) in light of previously described plasticity in body size and thermotolerance under these temperature and pCO2 treatments. Results: Although transcriptomic patterns primarily varied by developmental stage, there were pronounced differences in gene expression as a result of the treatment conditions. Temperature and pCO2 treatments led to the differential expression of genes related to the cellular stress response, transmembrane transport, metabolic processes, and the regulation of gene expression. At each developmental stage, temperature contributed significantly to the observed variance in gene expression, which was also correlated to the phenotypic attributes of the embryos. On the other hand, the transcriptomic response to pCO2 was relatively muted, particularly at the prism stage. (Continued on next page) * Correspondence: [email protected] 1Department of Ecology, Evolution and Marine Biology, University of California Santa Barbara, Santa Barbara, CA 93106, USA 2Present address: Department of Biological Sciences, Florida International University, North Miami, FL 33181, USA © The Author(s). 2021 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Wong and Hofmann BMC Genomics (2021) 22:32 Page 2 of 21 (Continued from previous page) Conclusions: M. franciscanus exhibited transcriptomic plasticity under different temperatures, indicating their capacity for a molecular-level response that may facilitate red sea urchins facing ocean warming as climate change continues. In contrast, the lack of a robust transcriptomic response, in combination with observations of decreased body size, under elevated pCO2 levels suggest that this species may be negatively affected by ocean acidification. High present-day pCO2 conditions that occur due to coastal upwelling may already be influencing populations of M. franciscanus. Keywords: Red sea urchin, Mesocentrotus franciscanus, RNA-seq, Transcriptomics, Early development, Climate change, Warming, Ocean acidification Background and early summer months [18–20]. Therefore, in the The red sea urchin Mesocentrotus franciscanus (A. Agas- CCS, M. franciscanus embryos and larvae experience siz, 1863) is an ecologically and economically valuable combinations of temperature and pH conditions that species found along the Pacific Coast of western North may vary depending on whether spawning and upwelling America [1]. In subtidal areas, especially within kelp for- events coincide. Furthermore, these urchins may be par- ests, these echinoderms are herbivorous ecosystem engi- ticularly vulnerable to stress during early development. neers that can shape the flow of resources within marine Although planktonic embryological and larval stages of habitats [2]. Overgrazing by M. franciscanus, often in echinoids are capable of exhibiting vertical migration combination with overgrazing by the purple sea urchin [21, 22], they are likely less capable of finding refuge Strongylocentrotus purpuratus, can lead to the formation from stressful conditions than their benthic adult coun- of urchin barrens in which macroalgal communities are terparts. There is also evidence that many organisms are severely reduced or depleted [3, 4]. Red sea urchins also most vulnerable to environmental stress early in their function as prey to animals at higher trophic levels, in- life history [23–26]. Both lethal and sublethal effects that cluding spiny lobsters and sea otters [5–7]. In addition occur during early development or that carry over into to its removal by natural predators, M. franciscanus is later life stages will negatively affect the recruitment ne- widely collected as a lucrative wild fishery species. Fish- cessary to support future populations [27, 28]. eries in Mexico, the United States, and Canada harvest Given the dynamic nature of their habitat and the pro- M. franciscanus for their gonads (i.e., roe) that supply gression of ocean warming and acidification, it is im- domestic markets as well as international exports, prin- perative to understand how early stage M. franciscanus cipally to Japan [8, 9]. Over recent years (2015–2019), respond to their environment on a molecular level. A the annual revenue reported from M. franciscanus fish- limited number of studies have investigated how M. eries across the states of California, Oregon, and Wash- franciscanus responds to temperature or pCO2 stress ington averaged over $7.1 million USD/year, far more [29–31], and even fewer have done so within a multi- than all other echinoderm fishery species combined [10]. stressor context [32]. In S. purpuratus, a species whose Given the considerable ecological and economic im- habitat largely overlaps with that of M. franciscanus, portance of M. franciscanus, determining how this spe- elevated temperatures and pCO2 levels during early cies will be affected by continuing environmental change development can cause increased mortality, abnormality, in coastal oceans remains an overlooked and critical area and a reduction in size and scope for growth [20, 33– of research [11]. Due to their habitat and life history, 35]. Several studies have identified and examined these urchins are threatened by climate change impacts temperature- and pCO2-responsive genes in S. purpura- [12] such as ocean warming, which may include sudden tus embryos and larvae [36–41]. Studies such as these and extreme marine heat waves [13, 14], and ocean acid- are essential for contributing molecular-level insights ification, which may amplify the low pH conditions that into how these organisms respond, or fail to respond, to episodically occur in upwelling regions [15]. The upwell- stressful environmental conditions and may help explain ing season in the California Current System (CCS) typic- effects observed at the level of the organism or popula- ally extends from early spring until late summer or fall; tion. This is particularly pertinent for fishery species in it is characterized by fluctuations between periods of up- which accurate predictions are necessary for adaptive, welling, when cold, low pH water is transported to the climate-ready fisheries management [42]. Although a surface, and periods in which upwelling is relaxed (i.e., clear understanding of how M. franciscanus responds to wind conditions are not conducive for driving upwelling) environmental stress is lacking, suggestions have already [16, 17]. This overlaps with the natural spawning period been made to replace or offset the M. franciscanus fish- of M. franciscanus that occurs annually during spring ery with Strongylocentrotus fragilis, a sea urchin species Wong and Hofmann BMC Genomics (2021) 22:32 Page 3 of 21 expected to be more tolerant to climate change [12]. understanding of how M. franciscanus development is Here, both temperature and pCO2 conditions were affected by current ocean conditions, as well as our pre- manipulated in a laboratory setting to investigate their dictive capacity of how this species will respond to fu- influence on the gene expression patterns of M. francis- ture ocean change. canus during its early development. To the best of our knowledge, this is the first study to use RNA sequencing Results (RNA-seq) to examine the M. franciscanus stress Summary statistics and overview of RNA-seq response. The samples used for RNA-seq were generated from In