Environmental transcriptomics under heat stress: Can environmental RNA reveal changes in gene expression of aquatic organisms?

• Published in: Molecular ecology
• Main Authors: Hechler, Robert M., Yates, Matthew C., Chain, Frédéric J. J., Cristescu, Melania E.
• Format: Journal Article
• Language: English
• Published: 04-10-2023
• ISSN: 0962-1083; 1365-294X
• DOI: 10.1111/mec.17152

Abstract
To safeguard biodiversity in a changing climate, taxonomic information about species turnover and insights into the health of organisms are required. Environmental DNA approaches are increasingly used for species identification, but cannot provide functional insights. Transcriptomic methods reveal the physiological states of macroorganisms, but are currently species‐specific and require tissue sampling or animal sacrifice, making community‐wide assessments challenging. Here, we test whether broad functional information (expression level of the transcribed genes) can be harnessed from environmental RNA (eRNA), which includes extra‐organismal RNA from macroorganisms along with whole microorganisms. We exposed
Daphnia pulex
as well as phytoplankton prey and microorganism colonizers to control (20°C) and heat stress (28°C) conditions for 7 days. We sequenced eRNA from tank water (after complete removal of
Daphnia
) as well as RNA from
Daphnia
tissue, enabling comparisons of extra‐organismal and organismal RNA‐based gene expression profiles. Both RNA types detected similar heat stress responses of
Daphnia
. Using eRNA, we identified 32
Daphnia
genes to be differentially expressed following heat stress. Of these, 17 were also differentially expressed and exhibited similar levels of relative expression in organismal RNA. In addition to the extra‐organismal
Daphnia
response, eRNA detected community‐wide heat stress responses consisting of distinct functional profiles and 121 differentially expressed genes across eight taxa. Our study demonstrates that environmental transcriptomics based on extra‐organismal eRNA can noninvasively reveal gene expression responses of macroorganisms following environmental changes, with broad potential implications for the biomonitoring of health across the trophic chain.