Comparative genomic analysis of obligately piezophilic Moritella yayanosii DB21MT-5 reveals bacterial adaptation to the Challenger Deep, Mariana Trench

Abstract

Hadal trenches are the deepest but underexplored ecosystems on the Earth. Inhabiting the trench bottom is a group of micro-organisms termed obligate piezophiles that grow exclusively under high hydrostatic pressures (HHP). To reveal the genetic and physiological characteristics of their peculiar lifestyles and microbial adaptation to extreme high pressures, we sequenced the complete genome of the obligately piezophilic bacterium Moritella yayanosii DB21MT-5 isolated from the deepest oceanic sediment at the Challenger Deep, Mariana Trench. Through comparative analysis against pressure sensitive and deep-sea piezophilic Moritella strains, we identified over a hundred genes that present exclusively in hadal strain DB21MT-5. The hadal strain encodes fewer signal transduction proteins and secreted polysaccharases, but has more abundant metal ion transporters and the potential to utilize plant-derived saccharides. Instead of producing osmolyte betaine from choline as other Moritella strains, strain DB21MT-5 ferments on choline within a dedicated bacterial microcompartment organelle. Furthermore, the defence systems possessed by DB21MT-5 are distinct from other Moritella strains but resemble those in obligate piezophiles obtained from the same geographical setting. Collectively, the intensive comparative genomic analysis of an obligately piezophilic strain Moritella yayanosii DB21MT-5 demonstrates a depth-dependent distribution of energy metabolic pathways, compartmentalization of important metabolism and use of distinct defence systems, which likely contribute to microbial adaptation to the bottom of hadal trench.

Biological functions at high pressure: transcriptome response of Shewanella oneidensis MR-1 to hydrostatic pressure relevant to Titan and other icy ocean worlds

“…HHP causes protein denaturation, alteration of protein functions, loss of membrane fluidity, loss of motility, and suppressed transcription/translation (reviews in Oger and Jebbar, 2010 ; Meersman et al, 2013 ; Mota et al, 2013 ; Silva et al, 2014 ). Despite these challenges, life has evolved to withstand high pressures, and organisms known as piezophiles have specific adaptations that allow them to grow more efficiently under HHP than at atmospheric pressure (e.g., Yayanos et al, 1979 ; Yayanos, 1995 ; Masanari et al, 2014 ; Peoples et al, 2020 ; Zhang et al, 2021 ). Adaptations to HHP identified from previous studies of piezophiles include increased protein flexibility (Martinez et al, 2016 ), increased abundance of heavy metal resistant genes (Zhang et al, 2021 ), and specialized chemotaxis, motility, and respiration systems (Michoud and Jebbar, 2016 ; Peoples et al, 2020 ).…”

“…Despite these challenges, life has evolved to withstand high pressures, and organisms known as piezophiles have specific adaptations that allow them to grow more efficiently under HHP than at atmospheric pressure (e.g., Yayanos et al, 1979 ; Yayanos, 1995 ; Masanari et al, 2014 ; Peoples et al, 2020 ; Zhang et al, 2021 ). Adaptations to HHP identified from previous studies of piezophiles include increased protein flexibility (Martinez et al, 2016 ), increased abundance of heavy metal resistant genes (Zhang et al, 2021 ), and specialized chemotaxis, motility, and respiration systems (Michoud and Jebbar, 2016 ; Peoples et al, 2020 ). The currently demonstrated growth limit at HHP is 140 MPa (Kusube et al, 2017 ), just below the 150 MPa pressure expected at the top of Titan's ocean.…”

“…The ability to grow more efficiently at high pressures is considered a highly specialized evolutionary trait (Yayanos, 1986 ; Bartlett, 1992 ; Zhang et al, 2021 ). Nonetheless, several reports have indicated that non-piezophiles, such as Shewanella oneidensis and Escherichia coli , can survive much higher pressures, up to 1.5 GPa for short periods of time (15 min) (Hauben et al, 1997 ; Griffin et al, 2011 ; Vanlint et al, 2011 ; Hazael et al, 2014 ).…”