Philippa Kaur

Intra-bull semen quality variationTo understand variation in bull semen quality, we assessed 1271 ejaculates from 79 different bulls (11 different breeds) housed at Rockhampton stud farm, in the state of Queensland, Australia, over a period of 5 years (2014–2018). The raw data, together with the semen analysis and when the samples for each individual bull were collected is available in Supplementary 1. The climate in this area (23.3786° S, 150.5089° E) is considered sub-tropical, ranging from 16 °C in winter to over 30 °C in summer. A comprehensive semen analysis was undertaken, including sperm morphology and motility. To determine the variation in semen quality, we plotted the percentage of sperm normal forms for each bull that had 5 or more ejaculates taken annually. Morphology was used as a measure of sperm quality, as Söderquist et al.17 demonstrated that sperm motility is heavily influenced by the collection/collectors and, therefore potentially unreliable and irreproducible. This resulted in the analysis of 1178 ejaculates from 50 bulls, with an average of 23 ejaculates per bull. The percentage of sperm normal forms as a box and whiskers plot for each bull is given (Fig. 1). As shown, many bulls demonstrated extremely high variation between ejaculates, with several males ranging from  70% (considered an outright “pass” in terms of cryopreservation potential) of normal sperm morphology. On the contrary, some bulls appeared to produce consistent semen samples across the year.Figure 1Changes in sperm normal forms. Semen samples were taken from bulls via electroejaculation and the percentage sperm normal forms were counted. The data show a box and whiskers plot consisting of 50 bulls, each of which had at least 5 different ejaculates across a minimum one month. Each box and whiskers plot represents an individual Bull showing the median, upper and lower quartile range. Outliers are represented by individual dots.Full size imageTo determine the amplitude and the proportion of bulls demonstrating variation in the number of normal sperm forms, we measured the difference between the maximum and the minimum values recorded for each animal. From this analysis we found that: 9 (18%) bulls showed less than 20% variation in normal forms; 15 (30%) bulls had between 20–40% variation; 13 (26%) bulls were between 40–60% and for 13 (26%) bulls this number was over 60%. These data have major implications when interpreting semen analysis, since a bull could be classified as either fertile or infertile depending on which ejaculate was considered. This data also sheds light into why correlations between the vBBSE parameters such as morphology and the bull fertility are so variable.Seasonal effect on semen qualitySeveral sources of environmental influence have been suggested to affect bull sperm quality. These include feed availability (i.e., higher conception rates in rainy seasons)27, excessive protein intake28, day length29, thermal heat stress and age30,31. To better understand the dynamics of semen quality variation within our samples, we plotted sample “pass” and “fail” cryopreservation criteria against the month of collection. A raw bull semen sample is classified as “pass” when motility is above 60% and normal forms greater than 70%. When samples were between 30 and 60% motility and 50–70% normal forms, they were classified as a “compensatory” (or qualified) pass (q-pass). The compensatory pass relied on there being the ability to have at least 10 million motile normal forms of spermatozoa in each straw to allow for conception. An outright failure was given to any sample with less than 30% progressive motility or 50% normal forms. This allowed each ejaculate to be placed into a binary “pass” or “fail”.The data for the percentage of total males that “failed” within each month (1271 ejaculates) is shown (Fig. 2A). Clearly, there is a seasonal pattern, with over 90% pass rate in winter (June–August) that fell to 50% or lower in summer (Dec-Feb). Considering that all bulls were greater than 4 years old, housed on the same stud farm and received the same dietary supplement we found no relationship in terms of “pass” or “fail” rates to these parameters. Thus, the data clearly suggested that Temperature/Temperature-Humidity or day length were responsible for the increased failure rates seen during Summer. Therefore, to understand if there was any causal relationship, we correlated either the average monthly temperature (Fig. 2B) or daylight (Fig. 2C) with monthly failure rates. The data showed a correlation with monthly temperature (r2 = 0.55; and temperature-humidity index – see further modelling below) but not with daylight hours (r2 = 0.05). Combined, these data suggest that temperature was the most likely reason for increased failure rates during the warm/hot months.Figure 2Seasonal variation in the semen quality of 1271 bull semen ejaculates. Semen samples were taken from bulls via electroejaculation and a full semen analysis was undertaken. Each sample was then classified as a pass or fail as described in Materials and Methods. (A) The percentage failure rate for each month is shown for all bulls. The number above each column indicate how many semen ejaculates were processed that month. (B). Scatter plot showing the average monthly temperature of Rockhampton and the percentage of samples that fail/month. Line of best fit indicates and r2 = 0.55. (C) Scatter plot showing the average daily sunlight in Rockhampton and the percentage of samples that fail/month. Line of best fit indicates and r2 = 0.04.Full size imageChanges in normal sperm forms categorised by breedThe present study investigated 11 different breeds of cattle, and we reasoned that maybe one, or more breed(s) contributed to failure rates more than others. Therefore, we plotted the percentage of normal forms for every ejaculate against the breed (Fig. 3). All breeds showed similar variation except for the Belmont Red, Boran and Wagyu. However, a relatively small number of bulls from the Belmont Red and Boran breeds were assessed in this study, therefore, it is unclear if they are indeed more resistant to heat. In the case of the Wagyu, it is worth mentioning that only one animal exhibited poor sperm morphology in several ejaculates (Fig. 3 circled) during winter. A close inspection of the records showed that during this time the animal had a fever episode, with body temperature reaching 39.4 °C, and that the sperm morphology returned to normal in approximately 70 days.Figure 3Variation in Semen quality as judged by Bull breed. Semen sample was collected and analysed for sperm morphology. The animals were then separated according to breed and the percentage normal forms for each ejaculate are shown.Full size imageSome bulls are heat-sensitive, whilst others are heat-tolerantAnalysis of the present data clearly illustrated that some bulls showed marked variation in terms of their semen quality throughout the year (Fig. 1). Meanwhile, others demonstrated much less variation, and were reasonably consistent. To further clarify these differences, we closely analysed the percentage of sperm morphology from two bulls, both of whom had several ejaculates were taken throughout the year, including during and after summer (Fig. 4). There was a clear pattern, and evidence of two types of bulls. Prior to the summer season, bull 1 (Fig. 4, red), designated here as “heat-sensitive”, exhibited  > 70% normal forms of spermatozoa. This value decreases dramatically, reaching its lowest point (10%) mid-January, before undergoing a recovery by April ( > 70%). In contrast, bull 2 (Fig. 4, green) showed a consistent semen profile throughout the year. The data suggest this bull was more “heat-tolerant”.Figure 4Identification of Heat-Sensitive and Heat-Tolerant bulls. The percentage normal sperm morphology from two bulls, both Droughtmasters, which had several ejaculates taken over the course of the year were plotted against the month in which the semen sample was taken. The first bull (red) is an example of a heat-sensitive bull. The second bull (Green) an example of heat-tolerant response.Full size imageTo further explore the concept of “heat-tolerant” and “heat-sensitive” bulls, we subjected 20 Wagyu bulls to a single event of controlled heat stress (40 °C, 12 h). This experiment was performed during Winter, at Singleton (New South Wales, Australia, 32.5695° S, 151.1788° E), where the average temperature was 17 °C and never exceeded 18 °C. Prior to the heat stress event, baseline semen samples were taken from each animal. After heat stress, semen samples were taken every week for 11 weeks. During the experiment, two bulls were removed from the program due to infection and sickness whilst a 3rd bull was removed as it refused to co-operate with electroejaculation procedure. From the remaining bulls, we were able to reproduce the heat-sensitive and heat-tolerant bull phenomenon. The raw data from this work is given in Supplementary 1, and an example of the data is shown (Fig. 5). For 14 bulls, we found no difference in terms of their baseline samples, which were between 70–90% normal forms. This is consistent with the Wagyu bull characteristics and their heat-tolerance (Fig. 5, yellow, green, blue lines). Within these “heat-tolerant” bulls, there was a variation of 16–22% sperm normal forms. For the other three bulls, two of them showed a decline in sperm quality, which began 2–3 weeks after the heat event, dropping from a baseline of 85% and 90% normal forms to 55% and 59%, respectively (30–31% variation in normal forms; Fig. 5, grey and orange line). The third bull showed a greater degree of heat-sensitivity. Starting at 77% morphologically normal sperm, the spermiogram of this bull illustrated a rapid decrease in normal forms in a short time (2 weeks), reaching around 40% after 4–5 weeks. Sperm morphology remained at this level (37% variation in normal form) for four weeks, before recovery. These data show that under experimental condition, the phenomenon of heat-sensitive and heat-tolerant animals can be reproduced. Further, it appears that there are degrees of heat-sensitivity.Figure 5Heating of Wagyu bulls to identify heat-sensitive and heat-tolerant effect. Twenty Wagyu bulls all 3 years of age and over were heated to 40 °C for 12 h in an insulated barn. Before heating, bassline samples were taken (week 1). After heating, electroejaculation was used to collect semen every week for 11 weeks. For every sample, sperm morphology was counted by a qualified theriogenologist. The data show the percentage normal morphology for 5 bulls. The light blue line indicates a heat-sensitive bulls, whose morphology was affected by heat, then returned back to baseline. The orange and grey line represent two related bulls (same father) who also produced less than 70% normal forms. The yellow, green and dark blue lines represent three heat-tolerant bulls, whose semen profile did not drop below the 70% normal spermatozoa threshold.Full size imageEnvironmental heat stress leads to poor sperm quality 17 days laterSimilar to previous reports, we noted that sperm quality does not begin to deteriorate until 2–3 weeks after the heat stress event of the bulls32. Based on the timing of spermatogenesis, this is consistent with reports that meiotic cells are more susceptible to heat stress following a heating event, with poor quality spermatozoa appearing in the ejaculate around 2–3 weeks later. To better understand the relationship between a “heat-event” and the production of poor-quality spermatozoa, we modelled both maximum temperature and maximum temperature humidity index (THI) and their relationship to the proportion of morphologically normal spermatozoa. The THI is an index representing the effect of humidity on the heat stress of an animal. THI was obtained using the following formula:$$mathrm{THI}=0.8* frac{{T}_{max}}{100}+frac{left(humidity*left({t}_{max}-14.4right)right)}{1}+46.4$$where Tmax = maximum temperature, (oF), and H = relative humidity.We plotted the correlation between semen quality and Tmax on the day, and every day prior (up to 40 days) to semen collection (Fig. 6). This modelling demonstrated that poor semen quality was due to maximum daytime temperature 17 days prior (Fig. 6a, arrow). Notably, 1 day of heat-stress appears to be sufficient to cause poor sperm quality, since if we take the average of 2 (Fig. 6b) or 3-day maximal temperatures prior to collection (Fig. 6c) the correlation patterns were similar. Supplementary 3 shows further modelling for Tmax and THI using between 1 and 5-day average temperatures prior to semen collection.Figure 6Bull semen quality (as percentage sperm normal forms) is related to the temperature that occurred 17–19 days ago. Correlation between sperm quality and maximum Temperature (Tmax). The Y axis is the Pearson correlation coefficient and X axis represents the number of days before the day the sperm sample was taken. (a) Uses one day of Tmax data whilst (b) averages two and (c) averages three consecutive days of Tmax data. The arrow shows the best correlation between Tmax and poor sperm quality, which occurs around 17–19 days before the semen sample is collected.Full size imageUnderstanding the temperatures at which heat-sensitive bulls failTo determine the Tmax at which bulls in the paddock begin to produce poor quality spermatozoa, we modelled data using both parameters measured at 17 days prior to the heat event, and plotted samples from 12 heat-sensitive bulls (6 Brahmans, 4 Drought Masters and 2 Santa Gertrudis). The relationship between sperm morphology and Tmax 17 days prior to heat even was plotted, with a spline smoothing cure to show the mean quality as a function of Tmax (Fig. 7a). As the temperature increase, so the quality of sperm morphology decreases as expected. To gain further clarity, we next fitted a nominal logistic regression analysis to model the proportion of spermatozoa that would either pass, Q-pass or fail sperm cryopreservation criteria as a function of Tmax 17 days prior. Tmax effect was highly significant for both outcome categories, with both p  More

Acidification of CPHistorical geochemical data suggest that the water chemistry of Cinder Pool (CP) has been relatively stable from the time of first reported geochemical data in 1947 until autumn 2018, followed by pronounced acidification between winter and spring 2019 (Supplementary Data 1, Fig. 1a, b). Images and documentation dating to even earlier (1927) reveal the presence of cinders covering ~50% of the spring surface at that time, a temperature near boiling (91.5 °C), and a description of having high sulfate and chloride levels (although data was not provided), suggesting that its chemistry has been generally stable since its discovery1. Spring pH ranged between ~3.6 and 4.5 in 22 yearly measurements spanning 71 years (1947–2018; multiple measurements in the same year were averaged to represent each year) (Fig. 1b), while the pH has been subsequently measured after 2018 as low as 2.5 (Fig. 1b). A single pH measurement of 2.5 was also recorded in a 2003 publication27, although other measurements in 2003, 2000, and 2001 were more consistent with the long-term average (i.e., pH 4.2–4.3; Supplementary Data 1). Scrutiny of chemical data accompanying the pH 2.5 measurement in 2003 indicates a SO42− concentration (~48 mg L−1) that is considerably lower than would be expected for CP, even when the pH is much higher (SO42− = 80 mg L−1; pH = 4.2–4.3). Considering that sulfuric acid is the predominant buffer of pH in these systems7,28, the pH 2.5 reading in 2003 is considered questionable. Nevertheless, the 2018 shift in pH towards more acidic conditions was accompanied by a notable change in the appearance of CP. Prior to autumn 2018, the spring waters were cloudy gray with the considerable suspension of kaolinite clay particles20 and black cinders10. However, between autumn 2018 and spring 2019, the spring waters visibly turned blue-green and contained colloidal S° particles that were also deposited along the pool shelves, while the pool also lacked its characteristic black cinders (Fig. 1a). The spring has maintained this appearance since spring 2019 until at least July 2022.Fig. 1: Historical geochemistry of Cinder Pool (CP).a Top panel shows the visual change in the appearance of CP in 2016 (left) and 2020 (right). Scale bars in the bottom right are ∼1 m. b Measurements of pH (n = 21; black line) and sulfate (SO42−) concentrations (n = 12; red line) in CP waters between 1947 and 2021. Years with multiple measurements were averaged to represent the entire year. c Paired measurements of SO42− and chloride (Cl−) concentrations (n = 12) between 1947 and 2021 in the context of the same measurements for 488 YNP springs derived from previous studies. Paired points for CP are colored based on the year they were recorded (averaged for multiple measurements/year as described above). End member fluid compositions as described in the manuscript text are indicated based on the abbreviations: MO meteoric only, HO hydrothermal only, MG meteoric plus gas, HB hydrothermal plus boiling, HBG hydrothermal plus boiling plus gas. Points for 2016, 2018, 2019, 2020, and 2021 are indicated by “16”, “18”, “19”, “20”, and “21”, respectively.Full size imageThe source of fluids in YNP hot springs can be broadly defined by concentrations of sulfate (SO42−) and chloride (Cl−)2,7. These indicators have been previously used to define the source of YNP springs as either (1) hydrothermal only (HO) waters that have moderate concentrations of SO42− (~30 mg L−1 depending on the depth of boiling; described below) but high concentrations of Cl− (~300 mg L−1), (2) meteoric-only (MO) waters containing lower concentrations of both solutes, or (3) MO waters infused with gas (MG) that have lower Cl− concentrations and higher SO42− concentrations (Fig. 1c). Subsequent boiling and/or evaporation of HO waters can concentrate Cl− and SO42− to higher concentrations (termed hydrothermal plus boiling; HB), while additional gas input into HO or HB waters can lead to particularly high concentrations of both Cl− and SO42− (hydrothermal + boiling + gas; HBG)7 (Fig. 1c). Geochemical data from surveys spanning 1947 to 2018 suggest that CP was largely sourced by hydrothermal (HO) waters that have undergone boiling and/or evaporation (HB) during this time frame (Fig. 1c).HO and HB waters are typically circumneutral7, while CP (which is also sourced by HB waters) has maintained a moderately acidic pH of ~4 until autumn 2018 (Fig. 1b). Several other low pH HB waters have been previously observed within the NGB7. The moderately acidic pH in CP (prior to 2018) has been attributed to the hydrolysis of molten S° that occurs at depths of >18 m that leads to the formation of S2O32– 11. Oxygen (O2)-dependent oxidation of S2O32−, catalyzed by trace iron sulfide in the cinders, forms SxO62− that can then react with sulfide to yield S2O32− and S° 11. Alternatively, SxO62− can be disproportionated to form S2O32− and SO42− 11. The relative rates of these reactions in CP prior to 2018 are not known although similar concentrations of S2O32− measured between 1995 and 1997 suggest that rates of S° hydrolysis and rates of S2O32− formation have been relatively constant over yearly time scales11. The consumption of O2 by reaction with S2O32− and the consumption of sulfide involving reactions with SxO62− would limit the amount of sulfuric acid that could be formed, thereby maintaining a less acidic pH than other sulfuric acid buffered acidic springs in YNP7.Between November 2018 and March 2019, the pH of CP markedly decreased to 2.8 in 2019, 2.7 in 2020, and 2.6 in 2021. This coincided with a marked increase in SO42− concentrations of ~3–5 fold above historical ranges (Fig. 1b), while Cl− concentrations fluctuated without clear trends during this time (Supplementary Fig. 1c). Thus, CP transitioned from an HB water type to an HBG water type between autumn 2018 and spring 2019 and has remained this way since (Fig. 1c). This is interpreted to reflect a substantial increase in H2S/S° oxidation that results in the formation of SO42− and H+ (sulfuric acid). Several observations suggest a fundamental restructuring of CP’s unique sulfur cycling due to dramatic physical and chemical changes at this time. As described in more detail below, the molten S° layer was detected at a depth of 18 m in 2016. However, in 2020 and 2021 there was no evidence of molten S° at ~18 to 20 m depth as previously documented, and sampling equipment could be freely dropped to a depth of 22 m (length of the cable) without interruption. In the absence of the molten S° at depth, the S° hydrolysis product S2O32−, and the cinders that catalyze SxO62− formation from S2O32− and H2S, it is possible that such reactions that previously competed for H2S or O2 (i.e., those involving S2O32− and SxO62−) are no longer taking place in CP. This in turn would allow for sulfur compounds (H2S and S°) to now be oxidized, thereby contributing to spring acidification.Alternative scenarios underlying the dramatic changes in CP waters also warrant consideration, and the three most logical are presented below. First, it is possible that the waters sourcing CP may have shifted either via replacement of the primary source or by altered mixing of multiple water sources. Water isotope values (δ2H and δ18O) can be used to further deconvolute the sources of hydrothermal waters because distinctive isotope values are associated with distinct water sources and the various influences upon them including meteoric water recharge, boiling (and/or evaporation), and water–rock interactions7,29. The water isotope values measured among the measured depths in CP in 2020 were near the range of water isotope values observed in CP across multiple months in 201613 (depth-resolved water isotope measurements were not made in 2016). The 2020 CP water isotope values were slightly right-shifted relative to those of 2016, suggesting a minor increase in the evaporation and concentration of CP water isotopes between 2016 and 20207 (Supplementary Fig. 2). These data thus do not support the hypothesis that the source of waters in CP dramatically shifted between 2016 and 2020, consistent with the SO42− and Cl− measurements indicating that the primary change to CP waters was increased input or availability of H2S for oxidation.A second alternative explanation is that a change in the water level of CP could potentially alter residence times which could allow for more oxidation of sulfur compounds in the spring and increased acidification. Such a scenario would also likely result in increased evaporation and concentration of solutes. However, the minimal increase in water isotope values (Supplementary Fig. 2) and similar Cl− concentrations (Supplementary Fig. 1c) accompanying a ~3–5 fold increase in SO42− concentration pre- and post-acidification (Fig. 1b) argue that increased residence time was of minimal importance in acidification.A third possible explanation is that a change in the plumbing system of CP is now delivering more vapor phase gas that contributes H2S and acidity when oxidized. Such a scenario could be consistent with increased surface deformation, subsurface gas accumulation, and seismic activity that has been taking place near NGB just prior to these changes21, and the transition from HB-type to HBG-type waters in CP. Sulfur species isotope analyses would help deconvolute the sources of SO42− in CP, but samples for sulfur isotopic analyses were not collected prior to acidification. Thus, it is unclear if this process may also be contributing to the acidification of CP. Regardless, the disappearance of the molten S° cap either by consumption or displacement would in effect make H2S more available for oxidation, similar to increased vapor phase input. The acidification of hot springs involves the oxidation of H2S by O230. More specifically, partial oxidation of H2S at acidic pH (90% amino acid identity to other homologs from UYS MAGs), but that was only present on unbinned contig sequences. Proteins are grouped based on their functionalities and associations in complexes. TetH (tetrathionate hydrolase), SQO sulfide:quinone oxidoreductase, SOR sulfur oxygenase reductase, SoxABCD Sulfolobus oxidase, SoxM Sulfolobus oxidase, CbsAB cytochrome b 558/566, SoxLN cytochrome ba complex, DoxBCE Desulfurolobus oxidase, DoxAD/TQOab Desulfurolobus oxidase/thiosulfate-quinone oxidoreductase, HdrAB1C1B2C2 (heterodisulfide reductase), DsrE3 DsrE3 sulfurtransferase, Dld dihydrolipoamide dehydrogenase, LplA lipoate-protein ligase A, LbpA lipoate binding protein A/glycine cleavage system H protein, TusA tRNA 2-thiouridine synthesizing protein A, SreABC sulfur reductase, SAOR sulfite:acceptor oxidoreductase, HcaLS [NiFe]-hydrogenase group 1 g. SoxEFGHI and FoxABCDEFGH (ferrous iron oxidation) gene sets were also investigated, but not identified in any of the MAGs and not shown here for brevity. A complete description of the enzymes/proteins found in individual UYS MAGs is provided in Supplementary Data 4.Full size imageTo assess the potential role of the UYS in sulfur biogeochemical cycling, the metabolic functional potentials of these populations were evaluated in greater detail based on their reconstructed genomes (Fig. 5, Supplementary Data 3). The UYS encoded the capacity for autotrophy via full complements of enzymes involved in the 3-hydroxypropionate/4-hydroxybutyrate cycle (3HP-4HB) (Supplementary Data 4), consistent with the general potential for autotrophy in most other Sulfolobales36. Consistently, the SoxM subunit that has been suggested as a marker for (facultatively) heterotrophic growth of Sulfolobales37 was absent in all UYS MAGs (Fig. 5, Supplementary Data 4). Given that all known Acidilobus and Vulcanisaeta spp. are characterized heterotrophs without known autotrophic capacity38,39, the UYS are likely the sole primary producers in the CP surface and subsurface waters, consistent with their considerable dominance in CP water communities over time.Also consistent with almost all other Sulfolobales36, the UYS universally encode the ability to reduce O2 via terminal cytochrome oxidases, although not via Sulfolobus oxidase (SoxABCD) complexes that are common among many Sulfolobales36 but rather via Desulfurolobus oxidase complexes (DoxBCE) (Fig. 5, Supplementary Data 4). An additional terminal oxidase complex (CbsAB-SoxLN) was encoded in the 2020 CP MAGs along with several other UYS MAGs from other YNP springs, although homologs of CbsAB-SoxLN were not present in the 2016 CP MAGs or several others recovered from sediments of other hot springs (Fig. 5). Thus, a potentially important metabolic difference between the pre- and post-acidification (2016 and 2020, respectively) CP Sulfolobales was the ability to use different terminal cytochrome oxidase compliments for aerobic respiration. The capacity to use multiple terminal oxidases has been suggested as an adaptation to varying oxygen tensions/availabilities37,40 that likely substantively differed between the low ORP 2016 CP waters and the high ORP 2020 CP waters (Fig. 2c). Consequently, these data point to the ecological succession of UYS strains within CP that are, at least in part, related to strain-level differences in aerobic respiration capacities.A defining feature of most cultured Sulfolobales is the ability to grow chemolithoautotrophically by coupling the oxidation of sulfur compounds (e.g., S0) to aerobic respiration37. The slow kinetics associated with abiotic oxidation of S0 with O2 at temperatures More

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