Abstract
Animal migrations mark the largest daily movement of biomass on Earth
today, but who performed the first diurnal migration? Extant benthic
microbial mats inhabiting Lake Huro’s low-oxygen, high-sulfur submerged
sinkholes that resemble life on early Earth, may offer some answers.
Herein, mats are dominated by motile filaments of purple-pigmented
cyanobacteria capable of oxygenic and anoxygenic photosynthesis, and
pigment-free chemosynthetic sulfur-oxidizing bacteria. We captured
time-lapse images of diurnal vertical migration between phototactic
cyanobacteria and chemotactic sulfur-oxidizing bacteria – dramatically
turning the mat surface purple at dawn and white at dusk. Alternating
waves of vertically migrating photosynthetic and chemosynthetic
filaments rapidly tracked diurnally fluctuating light; observations
corroborated with intact mats under simulated day-night conditions. Both
types of filaments increased in surface coverage non-linearly, albeit at
different rates. During their respective surface takeovers, maximum
nightly rate of movement for white chemosynthetic filaments occurred an
hour before that of purple cyanobacteria during the day. However, though
slow to start at dawn, the cyanobacteria’s maximum rate of movement was
double that of the chemosynthetic bacteria, leading to greater total
coverage over the span of the day. Such synchronized diurnal “tango”
might have been the largest daily mass movement of life during the long
Archean and Proterozoic eras, when the biosphere was mostly benthic, and
played a critical role in optimizing photosynthesis, chemosynthesis,
carbon burial, and oxygenation. Further studies of extant microbial
“mat worlds” will add to the expanding knowledge of Earth’s
biodiversity and physiologies, and may aid our ongoing search for life
in extraterrestrial waters.