The anhydrobiotic potential and molecular phylogenetics of species and strains ofPanagrolaimus(Nematoda, Panagrolaimidae)

Abstract

SUMMARY Members of the genus Panagrolaimus are bacterial-feeding nematodes that occupy a diversity of niches ranging from Antarctic and temperate soils to terrestrial mosses. Some members of this genus are able to survive extreme desiccation by entering into a state of suspended animation known as anhydrobiosis. We have assembled a collection of Panagrolaimusspecies and strains and have investigated their anhydrobiotic phenotypes. Our data show that within the genus Panagrolaimus there is a continuum of strains ranging from those unable to survive exposure to low relative humidity(RH) without prior preconditioning at high RH (slow desiccation strategists),through strains that have limited ability to survive rapid desiccation but whose anhydrobiotic ability improves upon preconditioning, to strains such as P. superbus that can readily survive immediate exposure to severe desiccation (fast desiccation strategists). Using this panel of nematodes we investigated the effect of preincubation at high RH on the accumulation of trehalose and on the nematodes' anhydrobiotic potential. We found that there is a strong correlation between trehalose induction and anhydrobiotic survival in Panagrolaimus. Furthermore, the high trehalose levels observed in fully hydrated P. superbus (10% dry mass) suggest that constitutive expression of trehalose pre-adapts this fast dehydration strategist to combat desiccation. All the strains observed, regardless of survival rates, undertook both coiling and clumping, which has the effect of reducing surface area and slowing the rate of water loss during desiccation. Phylogenetic analyses were carried out to investigate whether the observed anhydrobiotic phenotypes were the result of convergent evolution or represented a single phylogenetic lineage. These analyses, derived from alignments of the rDNA ITS and D3 sequences, indicate that the strongly anhydrobiotic strains of Panagrolaimus form a single phylogenetic lineage, which is separate from the weakly anhydrobiotic strains. The weakly anhydrobiotic strains are also phylogenetically divergent from each other. Our data indicate that Panagrolaimus has the potential to be an excellent model system for the investigation of molecular aspects of nematode anhydrobiosis.

Extreme resistance of bdelloid rotifers to ionizing radiation

“…This ability sets them apart not only from the great majority of other animal species, which are incapable of anhydrobiosis at any life stage, but also from the few that survive desiccation only when in a special relatively dormant stage, such as the larvae of the chironomid insect Polypedilum vanderplanki, the embryonic cysts of brine shrimps, and the resting eggs of monogonont rotifers (3)(4)(5). Bdelloids are further distinguished from certain species of nematodes and tardigrades that also tolerate desiccation at any life stage by not producing trehalose, a nonreducing disaccharide that is thought to contribute to the protection of cellular constituents against desiccation damage (6)(7)(8).…”

MAPK phosphorylation is implicated in the adaptation to desiccation stress in nematodes

“…In contrast, fast desiccation strategists such as Panagrolaimus superbus do not require preconditioning and can enter an anhydrobiotic state immediately on exposure to very dry conditions. It is thought that these organisms constitutively produce protective molecules; for example, P. superbus contains high levels of trehalose, up to 10% of dry weight, even when fully hydrated (Shannon et al, 2005;Tyson et al, 2012). Alternatively, slow desiccation strategists have also been described as external dehydration strategists because their rate of water loss is related to the relative humidity of their environment, while fast desiccation strategists have been termed innate dehydration strategists as it is thought they can control their rate of water loss to allow them more time to induce biochemical adaptations (Perry and Moens, 2011).…”

Volume and morphology changes of a bdelloid rotifer species (Macrotrachela quadricornifera) during anhydrobiosis

“…Bdelloids and tardigrades contract longitudinal muscles, retract head and foot into the trunk and form a compact ''tun'' shape (Wright, 2001;Ricci et al, 2003). Nematodes, incapable of significant body shortening, coil into tight spirals (Wharton, 1996;Womersley et al, 1998;Shannon et al, 2005). Both the tun and the compact spiral body forms reduce the surface area, which probably reduces the rate of water loss (Wright et al, 1992;Wright, 2001).…”