Antarctic haloarchaea – a unique Microbiome

Research on genomic variation of Antarctic haloarchaea provides insight into replicon structuring and biogeographic patterning of variation.
Published in Microbiology
Antarctic haloarchaea – a unique Microbiome

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The paper in Microbiome is here:

Haloarchaea are members of the domain Archaea that thrive in hypersaline environments. In Antarctica, the most well characterized haloarchaea come from a deep (36m), cold (as low as -20°C), marine-derived system called Deep Lake (DeMaere et al PNAS 2013). The lake is home to a low complexity community of microorganisms that is dominated by species of haloarchaea (Halohasta litchfieldiae [tADL], DL31 and Halorubrum lacusprofundi) that don’t tend to dominate in lower latitude systems. By environmental microbiology standards (where the majority of indigenous microbes are recalcitrant to laboratory isolation attempts), Hrr. lacusprofundi is exceptional in being amenable to isolation and cultivation. The ability to obtain new strains of the species have already proven to be of immense value with strain R1S1 providing the discovery of the plasmid (pR1SE) that ‘masquerades’ as a virus and disseminates via membrane vesicles (see Nature Research Microbiology Community); Erdmann et al Nat Microbiol 2017). 

The Antarctic haloarchaea from Deep Lake have also been found to be quite ‘promiscuous’, capable of sharing long (up to 35kb), high identity (~100% nucleotide identity) regions (HIRs) of DNA (DeMaere et al PNAS 2013). The ability to do so has interesting implications for the ‘pan-genome’ of haloarchaeal species – i.e. the total pool of genetic material comprised by all members of a species (Tettelin et al PNAS 2005). Given the dominant Deep Lake Antarctic haloarchaeal species differ to those elsewhere in the world, questions arise as to the extent and uniqueness of the Antarctic haloarchaeal pan-genome.  

In a study just published in Microbiome we set about defining differences between Hrr. lacusprofundi strain R1S1 (from Rauer 1 Lake) and strain ACAM34 (from Deep Lake). The strains provided the capacity to compare isolates from lakes located in different sectors of the East Antarctica region (one of 16 distinct ice-free biogeographic regions of Antarctica – Terrauds and Lee Diversity Distrib 2016): Rauer 1 Lake from Filla Island in the Rauer Island group, and Deep Lake ~ 30 km away and ~9 km ENE from Davis Station in the Vestfold Hills (image 1). 

The analysis of strain variation formed the last chapter of Bernhard Tschitschko’s PhD studies. His analysis coincided with data beginning to churn out from our JGI Community Science Program that was (and still is) producing metagenome data from samples taken during a major 2013-2015 over-wintering expedition along with some others samples from 2006 and 2008. As a result, Bernhard and others (from my group, JGI and UTS) were able to analyse metagenome data generated from four hypersaline Rauer Island lakes (Rauer 1, 3, 6 and 13), Club Lake (which neighbours Deep Lake) and a Deep Lake time series (2006, 2008, 2013-2014). This enabled assessments of population level genomic variation including the prevalence of strain specific genomic markers, and biogeographic patterns of genome evolution. 

Because the work involved a very detailed analysis of genomic content and variation through to a comparative assessment of communities across disparate lake systems, the types of outcomes realized from the study were quite varied. For example, Bernhard found that the way that haloarchaea accommodate genomic variation relates to replicon structuring (image 2). Different species of haloarchaea have one replicon (chromosome) or multiple replicons (one large primary replicon and one or more secondary replicons). Bernhard determined that haloarchaea which have a high proportion of their genome contained in secondary replicons have a proportionately lower content of genomic variation in their primary replicon (and vice versa). 

Consistent with Bernhard's previous study (Tschitschko et al ISMEJ 2015), he found that most of the Hrr. lacusprofundi strain variation could be associated with host-virus interactions (evasion/defence), with an interesting feature being the presence of an entire CRISPR/Cas region (~9.4 kb) representing a shared HIR with DL1 (a low abundance Halobacterium species). The study was also the first to use an Antarctic virus (isolated by Suzanne Erdmann) to perform infection studies on the two strains of Hrr. lacusprofundi, determining that one strain was easily infected and lysed, while the other strain was resistant.

In terms of grander implications, the study showed that specific haloarchaeal species were major species across the Rauer Islands and Vestfold Hills hypersaline lake systems (image 3).

The dominant haloarchaeal populations possessed a high level of genomic conservation and also exhibited biogeographic distinctions (image 1 & 4).

This indicates that these species are overall endemic to the Vestfold Hills-Rauer Islands and may very well be endemic to Antarctica. Very little is known about the endemism of Antarctic microorganisms (Cavicchioli Nat Rev Microbiol 2015): do regional distinctions occur (i.e. between the 16 distinct ice-free regions)?; does Antarctica have its own ‘total microbial pan-genome’ that varies to the rest of the world?; what does the extent of endemism mean for species invasion? – will the Antarctic populations be susceptible to alien species and hence ecosystem function become irrevocably perturbed? – one of our earlier studies suggests this could be the case for viral invasion of keystone bacterial species in Ace Lake (Lauro et al ISMEJ 2011). 

Antarctic wildlife has some very real and profound issues to deal with. Antarctic waters are already experiencing pollution (plastics, drugs, wastes) and a high risk of invasive species and diseases due to several million people visiting per year (tourism, fisheries, research stations). In a focus issue of Nature on Antarctica, it was highlighted that Antarctica has in fact lost its ‘pristine’ status due to untoward human behaviour (Nature Editorial 2018). Hopefully it is studies like ours that will help to document just how much natural wonder exists and waits to be discovered in Antarctica – there are all the right reasons in the world to motivate sensible politics towards providing real and lasting protection for this unique, polar environment (Cavicchioli Greenpeace).

Article poster image photo credits: Alyce Hancock, Sarah Payne, Rick Cavicchioli

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