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

James A Raymond,Daniel Remias

doi:10.3389/fmicb.2019.02697

Abstract

All ice-associated algae examined so far have genes for ice-binding proteins (IBPs), which suggest that these proteins are essential for survival in icy habitats. The most common type of IBP, type 1 IBPs (also referred to as DUF3494 IBPs), is also found in ice-associated bacteria and fungi. Previous studies have suggested that algal IBP genes were acquired by horizontal transfer from other microorganisms (probably bacteria). However, it remains unclear whether this is also the case for algae distantly related to the ones examined so far and whether microorganisms other than bacteria could be the donors. Furthermore, there is only limited evidence that these proteins are expressed at low temperature. Here, we show that Kremastochrysopsis austriaca (Chrysophyceae), an Austrian snow alga that is not closely related to any of the ice-associated algae examined so far, also produces IBPs, although their activity was weak. Sequencing the algal genome and the transcriptomes of cells grown at 1 and 15°C revealed three isoforms of a type 1 IBP. In agreement with their putative function, the three isoforms were strongly upregulated by one to two orders of magnitude at 1°C compared to 15°C. In a phylogenetic tree, the K. austriaca IBPs were distant from other algal IBPs, with the closest matches being bacterial proteins. These results suggest that the K. austriaca IBPs were derived from a gene that was acquired from a bacterium unrelated to other IBP donor bacteria and confirm by their presence in yet another alga the essential role of algal IBPs.

Highlights

Ice-binding proteins (IBPs) are produced and secreted by many ice-associated microorganisms 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)
Algal IBP genes appear to have been acquired from bacteria for several reasons: (1) the closest matches to algal IBPs are bacterial proteins, (2) IBP homologs are widely distributed in bacteria and have not been found in the genomes of mesophilic algae, and (3) the phylogeny of algal IBPs is largely independent of algal taxonomy (Raymond and Kim, 2012)
We show that K. austriaca has at least three isoforms of a type 1 (DUF3494) IBP that appear distant from other type 1 algal IBPs and that were most likely acquired from a bacterial gene

Summary

INTRODUCTION

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 Rather, they serve to mitigate damage from external ice by altering its structure and inhibiting its. A new species of snow alga, Kremastochrysopsis austriaca, was identified in the Austrian Alps (Remias et al, 2019) It is a chrysophyte (Stramenopiles), a class that has not been previously investigated with respect to IBPs. After finding evidence of IBP activity in a cell culture (pitting of the surface of an ice crystal growing in the culture medium), we sequenced the genome and transcriptomes of the alga incubated at 1 and 15°C to hunt for the IBP genes. The new results, combined with previous results, point to a possible difference between marine and freshwater IBPs

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DISCUSSION