Macrobiotus is a genus of tardigrades consisting of about 100 species within the family Macrobiotidae. Of genera within the phylum Tardigrada, Macrobiotus is one of the most species-abundant. Macrobiotus hufelandi, identified by German researcher Carl August Sigismund Schultze in 1834, is recognized as the first taxonomically named tardigrade species. By extension, Macrobiotus was the first ever described tardigrade genus. Macrobiotus shares similarities to other tardigrade genera, particularly in moulting a non-living cuticle over multiple life stages and robust stress tolerance mechanisms. However, Macrobiotus tends to be differentiated from other tardigrades by being one of few genera that freely lay ornamented eggs in reproduction. This genera has a relatively diverse distribution in both terrestrial and aquatic environments.
Anatomy and Morphology
Claws Macrobiotus species commonly exhibit uniform diploclaws on their legs.
Cuticle Macrobiotus belong to the clade Ecdysozoa, characterized for non-living cuticle layers that can be moulted over various life stages. This cuticular exoskeleton layer facilitates gas and water exchange. Protective benefits of the cuticle typically outweigh the energy costs required to moult.
Nervous System Macrobiotus neurons innervate a brain with inner and outer connectives, the latter connecting the brain to the trunk. Anterior leg nerves, posterior leg nerves, and peripheral nerves branch off of trunk ganglia. Connectives bridge adjacent trunk ganglia, and interpedal commissures bridge adjacent connectives.
Other Physiological Features Many Macrobiotus species also share a firm buccal tube containing a ventral lamina without a ventral hook, a pharynx with one microplacoid and two macroplacoids, and tend to exhibit 10 peribuccal lamellae.
Habitat and Distribution
Habitat Macrobiotus tend to inhabit limnoterrestrial habitats primarily consisting of mosses, though some Macrobiotus have also been discovered near lichens or aquatic plants. Some species of Macrobiotus are obligatory freshwater invertebrates. +Known Global Distribution of MacrobiotusContinentRegionAfricaSouth West AfricaTanzaniaAntarcticaSub-Antarctic IslandsAsiaChinaIsraelKyrgyzstanMalaysiaEuropeFinlandGermanyPortugalSwedenNorth AmericaCanadaGreenlandSouth AmericaBrazilFrench Guiana
Diet Macrobiotus sapiens is an example of a herbivorous diet consisting of algae.
Behaviour
Reproduction
Macrobiotus species exhibit a unique style of ornamented egg morphology and deposition process of freely laying ornamented eggs, contrasting to the ancestral state of freely laying smooth eggs. This is a synapomorphy of two families, Eohypsibioidea and Macrobiotidae, with Macrobiotoidea including the genus Macrobiotus. Ornamented eggs can limit water evaporation due to surface tension between water molecules and the egg's ornamentation.
Free-laying of eggs also differs from other common reproductive tendencies for tardigrades, whereby the old cuticle (or the exuvia) is used as an 'egg keeper' to allow egg development after laying. It is hypothesized that releasing eggs into the environment reduces predation of embryonic Macrobiotus species, providing an evolutionary advantage compared to laying eggs in only one place within the exuvia.
Partner finding behaviour occurs for freely-ovipositing Macrobiotus shonaicus species, where the male touches a female tardigrade's cloaca with their mouth several times, finishing their courtship ritual once the female tardigrade stops moving. Freely-ovipositing species are thought to identify partners using pheromones to accommodate only having simple light detection abilities.
Some free-laying egg species like M. shonaicus utilize chemotaxis for spermatozoa released during ejaculation to identify and swim towards the female's cloaca. Eggs are typically laid shortly after reproduction by the female, ranging from 16 minutes to 2 days after mating.
Macrobiotus exhibits bisexual achiasmy, whereby the process of crossing-over of genetic information between homologous chromosomes in meiosis is absent in both the male and female sex.
Stress Response
Anhydrobiosis Macrobiotus can withstand desiccation conditions by entering a state of anhydrobiosis. Compared to other tardigrades, Macrobiotus displays a moderate degree of desiccation tolerance. Some species have been observed to accumulate trehalose during anhydrobiotic states. Trehalose can induce the anhydrobiotic state, serving as a potential energy source while also protecting cellular membranes and proteins in freezing and desiccation conditions. Survival during anhydrobiosis depends on body size, particularly the size of energy-storing storage cells, though the reproductive state of oocyte maturation has no effect. It is predicted that the exoskeletal cuticle likely facilitates anhydrobiosis.
Some Macrobiotus may also demonstrate an encysted state primarily during periods of rest, but also metabolic depression.
Starvation One example species, M. sapiens, forms storage cells within their internal cavity in response to reduced food availability. This strategy helps Macrobiotus species survive for several weeks without food, during which storage cell sizes significantly decrease.
Moulting Macrobiotus, like other tardigrades, requires periodic moutling of their cuticle exoskeleton to grow in size. Cuticle lining the foregut independently moults first and is expelled through the mouth, followed by moutling the cuticles lining the exterior body and hindgut. Moulting may occur in response to poor environmental conditions or starvation as overall body size decreases.
Both male and female partners of M. shonaicus, a freely-ovipositing species, moult immediately before reproduction, moulting during the process of developing mature oocytes.
Species
The genus includes the following species:
Macrobiotus acadianus (Meyer & Domingue, 2011) Macrobiotus almadai Fontoura, Pilato & Lisi, 2008 Macrobiotus alvaroi Pilato & Kaczmarek, 2007 Macrobiotus anderssoni Richters, 1907 Macrobiotus andinus Maucci, 1988 Macrobiotus anemone Meyer, Domingue & Hinton, 2014 Macrobiotus annewintersae Vecchi & Stec, 2021 Macrobiotus ariekammensis Węglarska, 1965 Macrobiotus azzunae Ben Marnissi, Cesari, Rebecchi & Bertolani, 2021 Macrobiotus basiatus Nelson, Adkins Fletcher, Guidetti, Roszkowska, Grobys & Kaczmarek, 2020 Macrobiotus birendrai Kayastha et al., 2021 Macrobiotus biserovi Bertolani, Guidi & Rebecchi, 1996 Macrobiotus caelestis Coughlan, Michalczyk & Stec, 2019 Macrobiotus caelicola Kathman, 1990 Macrobiotus canaricus Stec, Krzywański & Michalczyk, 2018 Macrobiotus caymanensis Meyer, 2011 Macrobiotus crenulatus Richters, 1904 Macrobiotus crustulus Stec, Dudziak & Michalczyk, 2020 Macrobiotus dariae Pilato & Bertolani, 2004 Macrobiotus deceptor Meyer, Hinton, Gladney & Klumpp, 2017 Macrobiotus denticulus Dastych, 2002 Macrobiotus diversus Biserov, 1990 Macrobiotus dolosus Bertolani et al., 2023 Macrobiotus drakensbergi Dastych, 1993 Macrobiotus dulciporus Roszkowska, Gawlak, Draga & Kaczmarek, 2019 Macrobiotus echinogenitus Richters, 1903 Macrobiotus engbergi Stec, Tumanov & Kristensen, 2020 Macrobiotus fontourai Bertolani et al., 2023 Macrobiotus furcatus Ehrenberg, 1859 Macrobiotus glebkai Biserov, 1990 Macrobiotus grandis Richters, 1911 Macrobiotus gretae Massa et al., 2021 Macrobiotus halophilus Fontoura, Rubal & Veiga, 2017 Macrobiotus hannae Nowak & Stec, 2018 Macrobiotus horningi Kaczmarek & Michalczyk, 2017 Macrobiotus hufelandi C.A.S. Schultze, 1834 Macrobiotus humilis Binda & Pilato, 2001 Macrobiotus hupingensis Yuan et al., 2022 Macrobiotus hyperboreus Biserov, 1990 Macrobiotus iharosi Pilato, Binda & Catanzaro, 1991 Macrobiotus insularis Pilato, 2006 Macrobiotus joannae Pilato & Binda, 1983 Macrobiotus julianae (Meyer, 2012) Macrobiotus kamilae Coughlan & Stec, 2019 Macrobiotus kazmierskii Kaczmarek & Michalczyk, 2009 Macrobiotus kirghizicus Tumanov, 2005 Macrobiotus kosmali Kayastha et al., 2023 Macrobiotus kristenseni Guidetti, Peluffo, Rocha, Cesari & Moly de Peluffo, 2013 Macrobiotus kurasi Dastych, 1981 Macrobiotus lazzaroi Maucci, 1986 Macrobiotus lissostomus Durante Pasa & Maucci, 1979 Macrobiotus longipes Mihelčič, 1971 Macrobiotus macrocalix Bertolani & Rebecchi, 1993 Macrobiotus maculatus Iharos, 1973 Macrobiotus madegassus Maucci, 1993 Macrobiotus mandalaae Pilato, 1974 Macrobiotus margoae Stec, Vecchi & Bartels, 2021 in Stec et al. 2021 Macrobiotus marlenae Kaczmarek & Michalczyk, 2004 Macrobiotus martini Bartels, Pilato, Lisi & Nelson, 2009 Macrobiotus mileri Stec, 2024 Macrobiotus modestus Pilato & Lisi, 2009 Macrobiotus muralis Bertolani et al., 2023 Macrobiotus naginae Vecchi et al., 2022 Macrobiotus naskreckii Bąkowski, Roszkowska, Gawlak & Kaczmarek, 2016 Macrobiotus nebrodensis Pilato, Sabella, D'Urso & Lisi, 2017 Macrobiotus nelsonae Guidetti, 1998 Macrobiotus noemiae Roszkowska & Kaczmarek, 2019 Macrobiotus noongaris Coughlan & Stec, 2019 Macrobiotus norvegicus Mihelčič, 1971 Macrobiotus occidentalis occidentalis Murray, 1910 Macrobiotus occidentalis striatus Dastych, 1974 Macrobiotus ocotensis Pilato, 2006 Macrobiotus ovovittatus Stec, 2024 Macrobiotus pallarii Maucci, 1954 Macrobiotus papei Stec, Kristensen & Michalczyk, 2018 Macrobiotus patagonicus Maucci, 1988 Macrobiotus paulinae Stec, Smolak, Kaczmarek & Michalczyk, 2015 Macrobiotus persimilis Binda & Pilato, 1972 Macrobiotus personatus Biserov, 1990 Macrobiotus peteri Pilato, Binda & Catanzaro, 1991 Macrobiotus pisacensis Kaczmarek, Cytan, Zawierucha, Diduszko & Michalczyk, 2014 Macrobiotus polonicus Pilato, Kaczmarek, Michalczyk & Lisi, 2003 Macrobiotus polyopus Marcus, 1928 Macrobiotus polypiformis Roszkowska, Ostrowska, Stec, Janko & Kaczmarek, 2017 Macrobiotus porifini Kuzdrowska, Mioduchowska, Gawlak, Bartylak, A. Kepel, M. Kepel & Kaczmarek, 2021 Macrobiotus primitivae de Barros, 1942 Macrobiotus psephus du Bois-Reymond Marcus, 1944 Macrobiotus pseudofurcatus Pilato, 1972 Macrobiotus pseudohufelandi Stec, Vecchi, Calhim & Michalczyk, 2021 Macrobiotus pseudopallarii Stec, Vecchi & Michalczyk, 2021 in Stec et al. 2021 Macrobiotus punctillus Pilato, Binda & Azzaro, 1990 Macrobiotus radiatus Pilato, Binda & Catanzaro, 1991 Macrobiotus ragonesei Binda, Pilato, Moncada & Napolitano, 2001 Macrobiotus ramoli Dastych, 2005 Macrobiotus rawsoni Horning, Schuster & Grigarick, 1978 Macrobiotus rebecchii Stec, 2022 Macrobiotus recens Cuénot, 1932 Macrobiotus richtersi Pilato, Binda & Catanzaro, 1991 Macrobiotus ripperi Stec, Vecchi & Michalczyk, 2021 in Stec et al. 2021 Macrobiotus rybaki Stec & Vecchi, 2021 in Vecchi & Stec 2021 Macrobiotus sandrae Bertolani & Rebecchi, 1993 Macrobiotus santoroi Pilato & D'Urso, 1976 Macrobiotus sapiens Binda & Pilato, 1984 Macrobiotus scoticus Stec, Morek, Gąsiorek, Blagden & Michalczyk, 2017 Macrobiotus semmelweisi Pilato, Binda & Lisi, 2006 Macrobiotus serratus Bertolani, Guidi & Rebecchi, 1996 Macrobiotus seychellensis Biserov, 1994 Macrobiotus shonaicus Stec, Arakawa & Michalczyk, 2018 Macrobiotus siderophilus Bertolani et al., 2023 Macrobiotus sottilei Pilato, Kiosya, Lisi & Sabella, 2012 Macrobiotus terminalis Bertolani & Rebecchi, 1993 Macrobiotus trunovae Biserov, Pilato & Lisi, 2011 Macrobiotus vanescens Pilato, Binda & Catanzaro, 1991 Macrobiotus vladimiri Bertolani, Biserov, Rebecchi & Cesari, 2011 Macrobiotus wandae Kayastha, Berdi, Miaduchowska, Gawlak, Łukasiewicz, Gołdyn & Kaczmarek, 2020 Macrobiotus wuyishanensis P. Zhang & X.-Z. Sun, 2014 Macrobiotus yunshanensis Yang, 2002
References