Evidence for geographic isolation and signs of endemism within a protistan morphospecies

Abstract

The possible existence of endemism among microorganisms resulting from and preserved by geographic isolation is one of the most controversial topics in microbial ecology. We isolated 31 strains of "Spumella-like" flagellates from remote sampling sites from all continents, including Antarctica. These and another 23 isolates from a former study were characterized morphologically and by small-subunit rRNA gene sequence analysis and tested for the maximum temperature tolerance. Only a minority of the Spumella morpho- and phylotypes from the geographically isolated Antarctic continent follow the worldwide trend of a linear correlation between ambient (air) temperature during strain isolation and heat tolerance of the isolates. A high percentage of the Antarctic isolates, but none of the isolates from locations on all other continents, were obligate psychrophilic, although some of the latter were isolated at low ambient temperatures. The drastic deviation of Antarctic representatives of Spumella from the global trend of temperature adaptation of this morphospecies provides strong evidence for geographic transport restriction of a microorganism; i.e., Antarctic protistan communities are less influenced by transport of protists to and from the Antarctic continent than by local adaptation, a subtle form of endemism.

FIG. 1.

Sampling sites. Samples originated from different locations in Europe, Asia, Australia, New Zealand, Hawaii, and Antarctica (A). Each dot represents a sampling area comprising several remote sampling sites. For instance, the Antarctic isolates originate from habitats in three different sampling areas (B). For details, see Table S1 in the supplemental material.

FIG. 2.

Neighbor-joining tree showing the affiliation of SSU rRNA gene sequences from Spumella isolates with the Chrysophyceae sensu stricto. The numbers at the nodes of the tree indicate the percentage of bootstrap values for each node out of 100 bootstrap resamplings (values above 50 are shown). The scale bar indicates 2% estimated sequence divergence.

FIG. 3.

Geographic pattern of temperature tolerance of Spumella-like flagellates. Maximum growth temperatures differ between strains but are generally within certain limits that relate to environmental temperature. Strains originating from Antarctica are represented by black symbols; those from other continents are represented by white symbols. For the latter there is a global linear correlation of increasing temperature tolerance with increasing environmental temperature (dashed lines). Antarctic strains deviate from this trend; i.e., the realized temperature adaptation (gray oval) is stronger than expected from the global trend (white oval). The size of the symbol indicates the number of strains for the respective condition; i.e., small symbols represent one strain, medium-sized symbols represent two or three strains; and large symbols represent five strains.