Multiple ice‐binding proteins of probable prokaryotic origin in an Antarctic lake alga, Chlamydomonas sp. ICE‐MDV (Chlorophyceae)

Abstract

Ice-associated algae produce ice-binding proteins (IBPs) to prevent freezing damage. The IBPs of the three chlorophytes that have been examined so far share little similarity across species, making it likely that they were acquired by horizontal gene transfer (HGT). To clarify the importance and source of IBPs in chlorophytes, we sequenced the IBP genes of another Antarctic chlorophyte, Chlamydomonas sp. ICE-MDV (Chlamy-ICE). Genomic DNA and total RNA were sequenced and screened for known ice-associated genes. Chlamy-ICE has as many as 50 IBP isoforms, indicating that they have an important role in survival. The IBPs are of the DUF3494 type and have similar exon structures. The DUF3494 sequences are much more closely related to prokaryotic sequences than they are to sequences in other chlorophytes, and the chlorophyte IBP and ribosomal 18S phylogenies are dissimilar. The multiple IBP isoforms found in Chlamy-ICE and other algae may allow the algae to adapt to a greater variety of ice conditions than prokaryotes, which typically have a single IBP gene. The predicted structure of the DUF3494 domain has an ice-binding face with an orderly array of hydrophilic side chains. The results indicate that Chlamy-ICE acquired its IBP genes by HGT in a single event. The acquisitions of IBP genes by this and other species of Antarctic algae by HGT appear to be key evolutionary events that allowed algae to extend their ranges into polar environments.

Ice-Binding Proteins in a Chrysophycean Snow Alga: Acquisition of an Essential Gene by Horizontal Gene Transfer

“…In other cultures of IBP-producing algae, including the snow alga Chloromonas brevispina (JR unpublished data) and an Antarctic lake Chlamydomonas (Raymond and Morgan-Kiss, 2017), many type 1 IBPs belonging to contaminating bacteria were found. In the present case, however, no bacterial IBP genes were found, despite the presence of many bacteria in the culture.…”

“…Ice-binding proteins (IBPs) are produced and secreted by many ice-associated microorganisms (bacteria, algae, and fungi) from both marine and freshwater environments (Davies, 2014; Bar Dolev et al, 2016; Guo et al, 2017; Raymond and Morgan-Kiss, 2017; Vance et al, 2019). Some authors refer to microorganismal IBPs as antifreeze proteins, but that is incorrect because, unlike fish and insect antifreeze proteins (Devries, 1983; Duman, 2015), microorganismal IBPs are produced at concentrations that are too low to appreciably lower the freezing point.…”

Presence and absence of light-independent chlorophyll biosynthesis among Chlamydomonas green algae in an ice-covered Antarctic lake

“…UWO241 [6,7] and Chlamydomonas sp. ICE-MDV [5,8]. Both are bona fide psychrophiles in that they can withstand intense cold but die at more moderate temperatures.…”

“…Fortunately, we were able to reach out to some colleagues who have carried out extensive next-generation sequencing on ICE-MDV (Ion Torrent sequencing using Hi-Q chemistry and a P1 chip as well as Illumina paired-end sequencing on a NextSeq500) and searched these data for evidence of DPOR. (Please see [8] for details on culture conditions, DNA isolation, and sequencing and assembly methods. )…”

Glycerol Is an Osmoprotectant in Two Antarctic Chlamydomonas Species From an Ice-Covered Saline Lake and Is Synthesized by an Unusual Bidomain Enzyme

“…Among its adaptation are a photochemical apparatus well-suited for a cold, saline and low light environment (Morgan et al, 1998), more fluid membranes (Morgan-Kiss et al, 2002) and ice-binding proteins (IBPs) to prevent freeze-thaw injury (Raymond and Morgan-Kiss, 2013). Less is known about Chlamy-ICE which was isolated more recently: it also possesses IBPs (Raymond and Morgan-Kiss, 2017) but appears to have differences in acclimatory ability compared to Chlamy-UWO (Cook et al, 2019). Much more is known about the cold adaptations of a closely-related Antarctic pyschrophile Chlamydomonas sp.…”