Research Article: First Insights into the Subterranean Crustacean Bathynellacea Transcriptome: Transcriptionally Reduced Opsin Repertoire and Evidence of Conserved Homeostasis Regulatory Mechanisms

Date Published: January 20, 2017

Publisher: Public Library of Science

Author(s): Bo-Mi Kim, Seunghyun Kang, Do-Hwan Ahn, Jin-Hyoung Kim, Inhye Ahn, Chi-Woo Lee, Joo-Lae Cho, Gi-Sik Min, Hyun Park, Peng Xu.

http://doi.org/10.1371/journal.pone.0170424

Abstract

Bathynellacea (Crustacea, Syncarida, Parabathynellidae) are subterranean aquatic crustaceans that typically inhabit freshwater interstitial spaces (e.g., groundwater) and are occasionally found in caves and even hot springs. In this study, we sequenced the whole transcriptome of Allobathynella bangokensis using RNA-seq. De novo sequence assembly produced 74,866 contigs including 28,934 BLAST hits. Overall, the gene sequences were most similar to those of the waterflea Daphnia pulex. In the A. bangokensis transcriptome, no opsin or related sequences were identified, and no contig aligned to the crustacean visual opsins and non-visual opsins (i.e. arthropsins, peropsins, and melaopsins), suggesting potential regressive adaptation to the dark environment. However, A. bangokensis expressed conserved gene family sets, such as heat shock proteins and those related to key innate immunity pathways and antioxidant defense systems, at the transcriptional level, suggesting that this species has evolved adaptations involving molecular mechanisms of homeostasis. The transcriptomic information of A. bangokensis will be useful for investigating molecular adaptations and response mechanisms to subterranean environmental conditions.

Partial Text

Subterranean fauna form below the surface of the earth. Hyporheic/groundwater environments are harsh for animals due to limited space, permanent darkness, low dissolved oxygen concentrations, and limited energy/food inputs. The environment includes two major ecosystems, namely stygofauna (aquatic and living in groundwater) and troglofauna (air-breathing and living in caves and voids) [1]. Particularly, subterranean fauna exhibit several ecological and physiological characteristics that are evolutionary adaptations to the extreme environmental conditions. These adaptations include a high tolerance to hypoxia, low metabolic rates, longevity, delayed maturity, smaller clutch size, and simple food webs with few trophic links [2, 3]. Also, many hyporheic/groundwater organisms show phenotypical or morphological convergence such as reduced pigment, poorly functioning eyes or eye loss, development of non-optic sensory organs, and/or relative lengthening of appendages [4]. Although species richness is relatively restricted in the subterranean fauna, groundwater habitats develop unique biodiversity [5]. The groundwater ecosystem is composed mainly of tiny crustaceans, oligochaetes, nematodes, acari, and molluscs that have small body sizes of < 1mm to several centimeters [6]. Due to limited distribution, poor competitive ability, and low reproduction, the hyporheic/groundwater ecosystem is particularly vulnerable to environmental stressors and anthropogenic contamination. The ability of A. bangokensis to survive in such extreme subterranean environments suggests that they have evolved adaptations by employing molecular homeostatic mechanisms. The relationships between animals and their hyporheic/groundwater environments are being investigated continuously, and transcriptomic sequencing of A. bangokensis, as a sentinel species, renders it an optimal model for studying molecular adaptation and response mechanisms to harsh environmental conditions. Although the transcriptional responses induced by environmental changes or the unique adaptive metabolism of A. bangokensis are not discussed in this study due to the limited samples from subterranean regions, the transcriptomic database and gene composition provide the basis for clarifying the adaptive and responsive metabolic pathways. Thus, further identification and confirmation of the functions of conserved genes or pathways as well as the dissection of the genetic architecture of response genes will be useful for the study of adaptive mechanisms in subterranean ecosystems.   Source: http://doi.org/10.1371/journal.pone.0170424